Megabase-Scale Inversion Polymorphism in the Wild Ancestor of Maize

Abstract

Chromosomal inversions are thought to play a special role in local adaptation, through dramatic suppression of recombination, which favors the maintenance of locally adapted alleles. However, relatively few inversions have been characterized in population genomic data. On the basis of single-nucleotide polymorphism (SNP) genotyping across a large panel of Zea mays, we have identified an 50-Mb region on the short arm of chromosome 1 where patterns of polymorphism are highly consistent with a polymorphic paracentric inversion that captures .700 genes. Comparison to other taxa in Zea and Tripsacum suggests that the derived, inverted state is present only in the wild Z. mays subspecies parviglumis and mexicana and is completely absent in domesticated maize. Patterns of polymorphism suggest that the inversion is ancient and geographically widespread in parviglumis. Cytological screens find little evidence for inversion loops, suggesting that inversion heterozygotes may suffer few crossover-induced fitness consequences. The inversion polymorphism shows evidence of adaptive evolution, including a strong altitudinal cline, a statistical association with environmental variables and phenotypic traits, and a skewed haplotype frequency spectrum for inverted alleles.T HE evolutionary role of chromosomal inversions has been studied in a wide array of organisms, from insects (Ayala et al. 2011;Stevison et al. 2011) to birds (Huynh et al. 2011) and plants (Hoffmann and Rieseberg 2008; Lowry and Willis 2010). Examination of inversion polymorphism was fundamental to the early study of selection and adaptive diversity, as well as the basis for understanding the maintenance of neutral polymorphism within populations (Dobzhansky 1950;Hoffmann et al. 2004). Homologous pairing of an inverted and a noninverted chromosome in heterozygotes leads to the formation of an inversion loop, and crossing over in an inversion loop can cause the formation of a dicentric chromosome and an acentric fragment at meiosis I, resulting in terminal deletions of the affected chromosome and gamete death at frequencies that correlate with the size of the inversion (Burnham 1962). Because of the difficulty of homologous pairing and the deleterious effects of homologous crossing over in inversions, inversions are typically observed to disrupt recombination in heterozygous individuals, leading to measurable effects on nucleotide sequence polymorphism, including the generation of extended linkage disequilibrium (LD). Inversion-induced LD has been reported in a variety of organisms, including humans (Bansal et al. 2007), Drosophila subobscura (Munte et al. 2005), and several other species (reviewed in Hoffmann and Rieseberg 2008). Strong differentiation between chromosomal arrangements (as measured by F ST ) has also been used as evidence of inversions in Drosophila (Andolfatto et al. 1999;Depaulis et al. 1999;Nóbrega et al. 2008).A variety of circumstances can favor the maintenance or spread of an inversion polymorphism. The inversion may be 2010), ...

The genetic architecture of leaf number and its genetic relationship to flowering time in maize

“…This c . 50‐Mb inverted arrangement was found to dramatically suppress recombination (Fang et al ., 2012) (Fig. 7b).…”

Genomic Signature of Adaptation to Climate in Medicago truncatula

“…The strong LD among candidates within this region suggests that this region may contain a large inversion. Chromosomal inversions can maintain sets of co-adapted alleles at multiple loci and have been implicated in adaptation to climate in other plants, including Mimulus (Lowry and Willis 2010), A. thaliana (Long et al 2013), and teosinte (Fang et al 2012;Pyhäjärvi and Hufford 2013).…”

Independent Molecular Basis of Convergent Highland Adaptation in Maize

“…mexicana (hereafter mexicana) is native to the highlands of central Mexico, where it is thought to have occurred since at least the last glacial maximum (Ross-Ibarra et al 2009;Hufford et al 2012a). Phenotypic differences between mexicana and the lowland parviglumis mirror those between highland and lowland maize (Lauter et al 2004), and population genetic analyses of the two subspecies reveal evidence of natural selection associated with altitudinal differences (Fang et al 2012;Pyhäjärvi et al 2013). Landraces in the highlands of Mexico are often found in sympatry with mexicana and gene flow from mexicana likely contributed to maize adaptation to the highlands .…”