Causes of heterozygosity excess: The case of Mexican populations of Populus tremuloides

doi:10.1016/j.pld.2024.12.006

Plant Diversity ›› 2025, Vol. 47 ›› Issue (03): 415-428.DOI: 10.1016/j.pld.2024.12.006

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Causes of heterozygosity excess: The case of Mexican populations of Populus tremuloides

Javier Hernández-Velasco^a,b, José Ciro Hernández-Díaz^c, Sergio Leonel Simental-Rodríguez^a, Juan P. Jaramillo-Correa^d, David S. Gernandt^e, José Jesús Vargas-Hernández^f, Ilga Porth^g, Roos Goessen^g, M. Socorro González-Elizondo^h, Matthias Fladungⁱ, Cuauhtémoc Sáenz-Romero^j, José Guadalupe Martínez-Ávalos^k, Artemio Carrillo-Parra^c, Eduardo Mendoza-Maya^a, Arnulfo Blanco-García^l, Christian Wehenkel^c

a. Programa Institucional de Doctorado en Ciencias Agropecuarias y Forestales, Universidad Juárez del Estado de Durango, Constitución 404 sur. Zona Centro, C. P. 34000, Durango, Mexico;
b. Universidad Intercultural de Baja California (UIBC), San Quintín, Baja California, C. P. 22930, Mexico;
c. Instituto de Silvicultura e Industria de la Madera, Universidad Juárez del Estado de Durango, Constitución 404 sur. Zona Centro, C. P. 34000, Durango, Mexico;
d. Departamento de Ecología Evolutiva, Instituto de Ecología, Universidad Nacional Autónoma de México, 04510, CDMX, Mexico;
e. Departamento de Botánica, Instituto de Biología, Universidad Nacional Autónoma de México. 3er. Circuito Exterior, Ciudad Universitaria, C. P. 04510, Coyoacán, CDMX, Mexico;
f. Postgrado en Ciencias Forestales, Colegio de Postgraduados, Montecillo, Texcoco, 56264, Estado de México, Mexico;
g. Institute for System and Integrated Biology (IBIS), Université Laval, Charles-Eugène-Marchand Pavilion, 1030 Avenue de la Médecine, Quebec City, G1V 0A6, Québec, Canada;
h. Instituto Politécnico Nacional, CIIDIR Unidad Durango, Sigma 119 Fracc. 20 de Noviembre II, 34234, Durango, Durango, Mexico;
i. Thünen Institute of Forest Genetics, Sieker Landstr. 2, D-22927, Grosshansdorf, Germany;
j. Instituto de Investigaciones sobre los Recursos Naturales (INIRENA), Universidad Michoacana de San Nicolás de Hidalgo (UMSNH). Av. San Juanito Itzícuaro s/n, Col. Nueva Esperanza, Morelia Michoacán, 58337, Mexico;
k. Instituto de Ecología Aplicada, Universidad Autónoma de Tamaulipas, División del Golfo 356, Col. Libertad, Ciudad Victoria, 87019, Mexico;
l. Facultad de Biología, Universidad Michoacana de San Nicolás de Hidalgo (UMSNH). Av. J. Mújica s/n, Ciudad Universitaria, Morelia, Michoacán, C. P. 58030, Mexico

Received:2024-04-16 Revised:2024-12-25 Online:2025-05-21 Published:2025-05-25
Contact: Christian Wehenkel,E-mail:wehenkel@ujed.mx
Supported by:
We thank the Mexican Consejo Nacional de Humanidades, Ciencias y Tecnologías (CONAHCYT) for the financial support provided to the first author to carry out his training in the Institutional Doctoral Program in Agricultural and Forestry Sciences (PIDCAF-UJED) with Scholarship No. 334852 and financial support with agreement number CONACYT-FRQ-2016: 279459 for the project “Genome-wide scans for detecting adaptation to climate and soil in Populus tremuloides as the most widely distributed tree species in North América”.

Causes of heterozygosity excess: The case of Mexican populations of Populus tremuloides

a. Programa Institucional de Doctorado en Ciencias Agropecuarias y Forestales, Universidad Juárez del Estado de Durango, Constitución 404 sur. Zona Centro, C. P. 34000, Durango, Mexico;
b. Universidad Intercultural de Baja California (UIBC), San Quintín, Baja California, C. P. 22930, Mexico;
c. Instituto de Silvicultura e Industria de la Madera, Universidad Juárez del Estado de Durango, Constitución 404 sur. Zona Centro, C. P. 34000, Durango, Mexico;
d. Departamento de Ecología Evolutiva, Instituto de Ecología, Universidad Nacional Autónoma de México, 04510, CDMX, Mexico;
e. Departamento de Botánica, Instituto de Biología, Universidad Nacional Autónoma de México. 3er. Circuito Exterior, Ciudad Universitaria, C. P. 04510, Coyoacán, CDMX, Mexico;
f. Postgrado en Ciencias Forestales, Colegio de Postgraduados, Montecillo, Texcoco, 56264, Estado de México, Mexico;
g. Institute for System and Integrated Biology (IBIS), Université Laval, Charles-Eugène-Marchand Pavilion, 1030 Avenue de la Médecine, Quebec City, G1V 0A6, Québec, Canada;
h. Instituto Politécnico Nacional, CIIDIR Unidad Durango, Sigma 119 Fracc. 20 de Noviembre II, 34234, Durango, Durango, Mexico;
i. Thünen Institute of Forest Genetics, Sieker Landstr. 2, D-22927, Grosshansdorf, Germany;
j. Instituto de Investigaciones sobre los Recursos Naturales (INIRENA), Universidad Michoacana de San Nicolás de Hidalgo (UMSNH). Av. San Juanito Itzícuaro s/n, Col. Nueva Esperanza, Morelia Michoacán, 58337, Mexico;
k. Instituto de Ecología Aplicada, Universidad Autónoma de Tamaulipas, División del Golfo 356, Col. Libertad, Ciudad Victoria, 87019, Mexico;
l. Facultad de Biología, Universidad Michoacana de San Nicolás de Hidalgo (UMSNH). Av. J. Mújica s/n, Ciudad Universitaria, Morelia, Michoacán, C. P. 58030, Mexico

通讯作者: Christian Wehenkel,E-mail:wehenkel@ujed.mx
基金资助:
We thank the Mexican Consejo Nacional de Humanidades, Ciencias y Tecnologías (CONAHCYT) for the financial support provided to the first author to carry out his training in the Institutional Doctoral Program in Agricultural and Forestry Sciences (PIDCAF-UJED) with Scholarship No. 334852 and financial support with agreement number CONACYT-FRQ-2016: 279459 for the project “Genome-wide scans for detecting adaptation to climate and soil in Populus tremuloides as the most widely distributed tree species in North América”.

Abstract

Abstract: The presence of heterozygous individuals in a population is crucial for maintaining genetic diversity, which can positively affect fitness and adaptability to environmental changes. While inbreeding generally reduces the proportion of heterozygous individuals in a population, polyploidy tends to increase the proportion. North American Populus tremuloides is one of the most widely distributed and ecologically important tree species in the Northern Hemisphere. However, genetic variation in Mexican populations of P. tremuloides, including the genetic signatures of their adaptation to a variety of environments, remains largely uncharacterized. The aim of this study was to analyze how inbreeding coefficient (F_IS) and ploidy are associated with clonal richness, population cover, climate and soil traits in 91 marginal to small, isolated populations of this tree species throughout its entire distribution in Mexico. Genetic variables were determined using 36,810 filtered SNPs derived from genome re-sequencing. We found that F_IS was approximately between 0 and -1, indicating an extreme heterozygosity excess. One key contributor to the observed extreme heterozygosity excess was asexual reproduction, although ploidy levels cannot explain this excess. Analysis of all neutral SNPs showed that asexual reproduction was positively correlated with observed heterozygosity (H_o) but negatively correlated with expected heterozygosity (H_e). Analysis of outlier SNPs also showed that asexual reproduction was positively correlated with H_o and negatively correlated with H_e, although this latter correlation was not significant. These findings support the presence of a Meselson effect.

Key words: Quaking aspen, Diploid, Triploid, Asexual reproduction, Adaptation, Deleterious SNPs

摘要： The presence of heterozygous individuals in a population is crucial for maintaining genetic diversity, which can positively affect fitness and adaptability to environmental changes. While inbreeding generally reduces the proportion of heterozygous individuals in a population, polyploidy tends to increase the proportion. North American Populus tremuloides is one of the most widely distributed and ecologically important tree species in the Northern Hemisphere. However, genetic variation in Mexican populations of P. tremuloides, including the genetic signatures of their adaptation to a variety of environments, remains largely uncharacterized. The aim of this study was to analyze how inbreeding coefficient (F_IS) and ploidy are associated with clonal richness, population cover, climate and soil traits in 91 marginal to small, isolated populations of this tree species throughout its entire distribution in Mexico. Genetic variables were determined using 36,810 filtered SNPs derived from genome re-sequencing. We found that F_IS was approximately between 0 and -1, indicating an extreme heterozygosity excess. One key contributor to the observed extreme heterozygosity excess was asexual reproduction, although ploidy levels cannot explain this excess. Analysis of all neutral SNPs showed that asexual reproduction was positively correlated with observed heterozygosity (H_o) but negatively correlated with expected heterozygosity (H_e). Analysis of outlier SNPs also showed that asexual reproduction was positively correlated with H_o and negatively correlated with H_e, although this latter correlation was not significant. These findings support the presence of a Meselson effect.

关键词: Quaking aspen, Diploid, Triploid, Asexual reproduction, Adaptation, Deleterious SNPs

Javier Hernández-Velasco, José Ciro Hernández-Díaz, Sergio Leonel Simental-Rodríguez, Juan P. Jaramillo-Correa, David S. Gernandt, José Jesús Vargas-Hernández, Ilga Porth, Roos Goessen, M. Socorro González-Elizondo, Matthias Fladung, Cuauhtémoc Sáenz-Romero, José Guadalupe Martínez-Ávalos, Artemio Carrillo-Parra, Eduardo Mendoza-Maya, Arnulfo Blanco-García, Christian Wehenkel. Causes of heterozygosity excess: The case of Mexican populations of Populus tremuloides[J]. Plant Diversity, 2025, 47(03): 415-428.

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Causes of heterozygosity excess: The case of Mexican populations of Populus tremuloides

Causes of heterozygosity excess: The case of Mexican populations of Populus tremuloides

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