Demonstration of local adaptation of maize landraces by reciprocal transplantation

Authors: JANZEN, GARRETT - Iowa State University; AGUILAR-RANGEL, MARIA ROCIO - Langebio Cinvestav; CINTORA-MARTINEZ, CAROLINA - Langebio Cinvestav; BLÖCHER-JUÁREZ, KARLA AZUCENA - Langebio Cinvestav; GONZALEZ-SEGOVIA, ERIC - Langebio Cinvestav; STUDER, ANTHONY - University Of Illinois; RUNCIE, DANIEL - University Of California, Davis; Flint-Garcia, Sherry; RELLAN-ALVAREZ, RUBEN - Langebio Cinvestav; SAWERS, RUAIRIDH - Langebio Cinvestav; HUFFORD, MATTHEW - Iowa State University

Submitted to: Evolutionary Applications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/31/2022
Publication Date: 5/1/2022
Citation: Janzen, G.M., Aguilar-Rangel, M., Cintora-Martinez, C., Blöcher-Juárez, K., Gonzalez-Segovia, E., Studer, A.J., Runcie, D.E., Flint Garcia, S.A., Rellan-Alvarez, R., Sawers, R.J., Hufford, M.B. 2022. Demonstration of local adaptation of maize landraces by reciprocal transplantation. Evolutionary Applications. 15(5):817-837. https://doi.org/10.1111/eva.13372.
DOI: https://doi.org/10.1111/eva.13372

Interpretive Summary: Corn was domesticated from its wild relative, teosinte, over 9000 years ago in southwestern Mexico. As primitive corn was carried across the Americas, farmers selected plants/seed for desirable characteristics and suitability for growth in their local environment, resulting in varietal populations called landraces, i.e. populations with defined plant, ear, and kernel characteristics. Landraces, including highland-adapted corn landraces, have useful trait variation that is difficult to use in breeding programs because of local adaptation (e.g. adaptation to short growing season, cooler temperatures, higher solar radiation). There were multiple independent adaptations to high elevation growing conditions, including in Mexico and South America. We evaluated a collection of 120 landraces (from Mexican lowlands and highlands, and South American lowlands and highlands) in both lowland and highland field sites in Mexico in order to determine which characteristics are associated with highland adaptation. As expected, we found that landraces had the highest fitness when grown at their original elevation: highland landraces performed best in the highland field site, and lowland landraces performed best in the lowland field site. Characteristics associated with adaptation included stalk pigmentation (highland landraces had more pigment, especially in the highland field site), stalk macrohairs (highland landraces tended to have more hairs, especially Mexican landraces), and water use efficiency (highland landraces were more efficient). This study verified that landraces have adapted to specific environments, including to the highland environment. Breeding with landraces can restore key genetic variants which have been lost in modern corn, and can impart adaptations to challenging environments. Therefore, understanding the process of local adaptation is critical to adapting our crops to the changing environment.

Technical Abstract: Populations are locally adapted when they exhibit higher fitness than foreign populations in their native habitat. Maize landrace adaptations to highland and lowland conditions are of interest to researchers and breeders. To determine the prevalence and strength of local adaptation in maize landraces, we performed a reciprocal transplant experiment across an elevational gradient in Mexico. We grew 120 landraces, grouped into four populations (Mexican Highland, Mexican Lowland, South American Highland, South American Lowland), in Mexican highland and lowland common gardens and collected phenotypes relevant to fitness and known highland-adaptive traits such as anthocyanin pigmentation and macrohair density. 67k DArTseq markers were generated from field specimens to allow comparisons between phenotypic patterns and population genetic structure. We found phenotypic patterns consistent with local adaptation, though these patterns differ between the Mexican and South American populations. Quantitative trait differentiation (QST) was greater than neutral allele frequency differentiation (FST) for many traits, signaling directional selection between pairs of populations. All populations exhibited higher fitness metric values when grown at their native elevation, and Mexican landraces had higher fitness than South American landraces when grown in these Mexican sites. As environmental distance between landraces’ native collection sites and common garden sites increased, fitness values dropped, suggesting landraces are adapted to environmental conditions at their natal sites. Correlations between fitness and anthocyanin pigmentation and macrohair traits were stronger in the highland site than the lowland site, supporting their status as highland-adaptive. These results give substance to the long-held presumption of local adaptation of New World maize landraces to elevation and other environmental variables across North and South America.