Molecular Parallelism Underlies Convergent Highland Adaptation of Maize Landraces

Author:

Wang Li123,Josephs Emily B45,Lee Kristin M3,Roberts Lucas M2,Rellán-Álvarez Rubén67,Ross-Ibarra Jeffrey38,Hufford Matthew B2

Affiliation:

1. Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China

2. Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, IA, USA

3. Department of Evolution and Ecology, University of California, Davis, Davis, CA, USA

4. The Ecology, Evolution, and Behavior Program, Michigan State University, East Lansing, MI, USA

5. Department of Plant Biology, Michigan State University, East Lansing, MI, USA

6. Langebio, Irapuato, Gto., Mexico

7. Department of Molecular and Structural Biochemistry, North Carolina State University, Raleigh, NC, USA

8. Genome Center and Center for Population Biology, University of California, Davis, Davis, CA, USA

Abstract

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.

Funder

National Natural Science Foundation of China

Shenzhen Science and Technology Program

Shenzhen Dapeng New District

U.S. Department of Agriculture

National Science Foundation

NSF

USDA Hatch projects

AMC-FUMEC 2017 Summer Stay Fellowship

Publisher

Oxford University Press (OUP)

Subject

Genetics,Molecular Biology,Ecology, Evolution, Behavior and Systematics

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