Independent Molecular Basis of Convergent Highland Adaptation in Maize

Abstract

Convergent evolution is the independent evolution of similar traits in different species or lineages of the same species; this often is a result of adaptation to similar environments, a process referred to as convergent adaptation. We investigate here the molecular basis of convergent adaptation in maize to highland climates in Mesoamerica and South America, using genome-wide SNP data. Taking advantage of archaeological data on the arrival of maize to the highlands, we infer demographic models for both populations, identifying evidence of a strong bottleneck and rapid expansion in South America. We use these models to then identify loci showing an excess of differentiation as a means of identifying putative targets of natural selection and compare our results to expectations from recently developed theory on convergent adaptation. Consistent with predictions across a wide parameter space, we see limited evidence for convergent evolution at the nucleotide level in spite of strong similarities in overall phenotypes. Instead, we show that selection appears to have predominantly acted on standing genetic variation and that introgression from wild teosinte populations appears to have played a role in highland adaptation in Mexican maize.KEYWORDS convergent evolution; highland adaptation; maize; population genomics C ONVERGENT evolution occurs when multiple species or populations exhibit similar phenotypic adaptations to comparable environmental challenges (Wood et al. 2005;Arendt and Reznick 2008;Elmer and Meyer 2011). Evolutionary genetic analysis of a wide range of species has provided evidence for multiple pathways that lead to convergent evolution. One such route occurs when identical mutations arise independently and fix via natural selection in multiple populations. In humans, for example, malaria resistance due to mutations from Glu to Val at the sixth codon of the b-globin gene has arisen independently on multiple unique haplotypes (Currat et al. 2002;Kwiatkowski 2005). Convergent evolution can also be achieved when different mutations arise within the same locus yet produce similar phenotypic effects. Grain fragrance in rice appears to have evolved along these lines, as populations across East Asia have similar fragrances resulting from at least eight distinct loss-of-function alleles in the BADH2 gene (Kovach et al. 2009). Finally, convergent evolution may arise from natural selection acting on standing genetic variation in an ancestral population. In the three-spined stickleback, natural selection has repeatedly acted to reduce armor plating in independent colonizations of freshwater environments. Adaptation in these populations occurred both from new mutations and from standing variation at the Eda locus in marine populations (Colosimo et al. 2005).Not all convergent phenotypic evolution is the result of convergent evolution at the molecular level, however. Recent studies of adaptation to high elevation in humans, for example, reveal that the genes involved in highland adaptation are largely dist...

Maize diversity associated with social origin and environmental variation in Southern Mexico

“…Research on the distribution of maize races in central Mexico (Perales et al, 2003) and Chiapas (Brush and Perales, 2007) found that maize races are distributed according to elevation, and common garden experiments suggest local adaptation to elevation (Mercer et al, 2008). van Heerwaarden (2007 showed close association between maize genetic structure and elevation at a regional scale in eastcentral Mexico, and genetic analyses find a significant impact of elevation on genome-wide diversity in both maize and its wild relative teosinte (Bradburd et al, 2013;Pyhäjärvi et al, 2013;Takuno et al, 2015). Contrary to these findings, we found no differentiation of maize populations by elevation (races, morphological traits and molecular markers), likely because of the much smaller geographic scale of our population sampling.…”

Signatures of local adaptation in lowland and highland teosintes from whole‐genome sequencing of pooled samples

“…) and 10 were previously identified as F ST outliers between lowland and highland maize in Mesoamerica (Takuno et al . ). We also confirmed the adaptive role of Inv1 with a cluster of 20 outlier SNPs falling within the inversion (Table ).…”

Genetic heterogeneity underlying variation in a locally adaptive clinal trait in Pinus sylvestris revealed by a Bayesian multipopulation analysis

“…Some adaptive traits have also been shown to be genetically heterogeneous, such as high altitude adaptation in humans (see, for example, Jeong and Di Rienzo, 2014) and highland adaptation in maize (Takuno et al, 2015). In these cases, however, the level of gene flow between the different sites of adaptation is lower than what is assumed between central and northern European populations of Scots pine.…”