Molecular Parallelism Underlies Convergent Highland Adaptation of Maize Landraces

Abstract

Convergent phenotypic evolution provides some of the strongest evidence for adaptation. However, the extent to which recurrent phenotypic adaptation has arisen via parallelism at the molecular level remains unresolved, as does the evolutionary origin of alleles underlying such adaptation. Here, we investigate genetic mechanisms of convergent highland adaptation in maize landrace populations and evaluate the genetic sources of recurrently selected alleles. Population branch excess statistics reveal substantial evidence of parallel adaptation at the level of individual single-nucleotide polymorphism (SNPs), genes, and pathways in four independent highland maize populations. The majority of convergently selected SNPs originated via migration from a single population, most likely in the Mesoamerican highlands, while standing variation introduced by ancient gene flow was also a contributor. Polygenic adaptation analyses of quantitative traits reveal that alleles affecting flowering time are significantly associated with elevation, indicating the flowering time pathway was targeted by highland adaptation. In addition, repeatedly selected genes were significantly enriched in the flowering time pathway, indicating their significance in adapting to highland conditions. Overall, our study system represents a promising model to study convergent evolution in plants with potential applications to crop adaptation across environmental gradients.

A B73×Palomero Toluqueño mapping population reveals local adaptation in Mexican highland maize

“…The flowering QTL qDTA8, qDTS8, and qASI8 overlap a ∼10-Mb region that contains the two well-characterized flowering genes ZmRap2.7 and Zcn8 . This region and/or these genes have been reproducibly detected in linkage- and association-mapping studies of maize flowering time ( Chardon et al 2004 ; Buckler et al 2009 ; Steinhoff et al 2012 ; Li et al 2016 ; Romero Navarro et al 2017 ), temperate adaptation ( Ducrocq et al 2008 ; Bouchet et al 2013 ; Guo et al 2018 ; Castelletti et al 2020 ), and adaptation to the Mexican Highlands ( Gates et al 2019 ; Janzen et al 2021 ; Wang et al 2021 ). An early flowering Vgt1 allele from northern germplasm has previously been associated with a miniature transposon (MITE) insertion upstream of ZmRap2.7 , although the absence of the MITE alone did not explain late flowering Vgt1 alleles ( Buckler et al 2009 ).…”

Characterization of Flowering Time in Genebank Accessions of Grain Amaranths and Their Wild Relatives Reveals Signatures of Domestication and Local Adaptation

“…Early flowering facilitates local adaptation also in high altitudes for similar reasons. Recently, Wang et al [55] reported the parallel evolution of early flowering phenotypes in four highland maize populations compared to two lowland populations that exhibited later flowering. This study also showed that many flowering time genes were selected during highland adaptation, including genes from the photoperiod-pathway and the circadian clock.…”

AF-vapeR: A multivariate genome scan for detecting parallel evolution using allele frequency change vectors

“…It is also of interest whether repeatability occurs through: 1) repeated selection at the same SNP (often termed 'parallel' evolution) (e.g. stickleback adapted to freshwater (Colosimo, 2005) and maize adapted to highlands (L. Wang et al, 2021); 2) nonidentical changes in the same genes or loci ('convergence' (e.g. repeated modification of Mc1r during pigmentation evolution (Manceau et al, 2010)); 3) changes in different genes of similar function ('functional convergence' (e.g.…”