Genomic Analyses of Wild and Cultivated Bacanora Agave (Agave angustifolia var. pacifica) Reveal Inbreeding, Few Signs of Cultivation History and Shallow Population Structure

Abstract

Due to the recent increase in demand for agave-based beverages, many wild agave populations have experienced rapid decline and fragmentation, whereas cultivated plants are now managed at monocultural plantations, in some cases involving clonal propagation. We examined the relative effect of migration, genetic drift, natural selection and human activities on the genetic repertoire of Agave angustifolia var. pacifica, an agave used for bacanora (an alcoholic spirit similar to tequila) production in northwestern Mexico. We sampled 34 wild and cultivated sites and used over eleven thousand genome-wide SNPs. We found shallow genetic structure among wild samples, although we detected differentiation between coastal and inland sites. Surprisingly, no differentiation was found between cultivated and wild populations. Moreover, we detected moderate inbreeding (FIS ~ 0.13) and similar levels of genomic diversity in wild and cultivated agaves. Nevertheless, the cultivated plants had almost no private alleles and presented evidence of clonality. The overall low genetic structure in A. angustifolia var. pacifica is apparently the result of high dispersibility promoted by pollinators and the possibility of clonal reproduction. Incipient cultivation history and reliance on wild seeds and plants are probably responsible for the observed patterns of high genetic connectivity and considerable diversity in cultivated samples.

Conservation genomics of Agave tequilana Weber var. azul: low genetic differentiation and heterozygote excess in the tequila agave from Jalisco, Mexico

“…The new sequencing technologies are now routinely used to discover a large number of single nucleotide polymorphisms (SNPs) ( Elshire et al, 2011 ; Barrera-Redondo, Piñero & Eguiarte, 2020 ; Eguiarte et al, 2022 ; Klimova et al, 2022 ). These new technologies have been particularly useful for plant species with complex and large genomes, such as agaves ( Eguiarte et al, 2013 , 2021 ).…”

“…For all the samples, genomic DNA was extracted from leaf tissue using a modified “Mini-Prep” CTAB protocol ( Doyle & Doyle, 1987 ; Klimova et al, 2022 ). DNA was visualized on a 1% agarose electrophoresis gel, and quantified using the Qubit 3.0 fluorometer with Qubit dsDNA broad-range kit and NanoDrop Lite Spectrophotometer by Thermo Fisher Scientific.…”

“…Genetic diversity in cultivated agaves varies according to the intensity of use, management, and domestication ( Eguiarte et al, 2013 , 2021 ; Trejo et al, 2018 ; Álvarez-Ríos et al, 2020 ; Klimova et al, 2022 ). In wild agaves, genetic diversity is usually high, with low genetic differentiation among populations (see reviews in Eguiarte et al, 2013 , 2021 ; Klimova et al, 2022 ), a pattern that is maintained in part by the most important agave pollinators, such as the nectarivorous bats, Leptonycteris nivalis and L. yerbabuenae ( Eguiarte, Souza & Silva-Montellano, 2000 ; Rocha et al, 2006 ; Trejo-Salazar, Scheinvar & Eguiarte, 2015 ; Eguiarte et al, 2021 ).…”

“…Genetic diversity in cultivated agaves varies according to the intensity of use, management, and domestication ( Eguiarte et al, 2013 , 2021 ; Trejo et al, 2018 ; Álvarez-Ríos et al, 2020 ; Klimova et al, 2022 ). In wild agaves, genetic diversity is usually high, with low genetic differentiation among populations (see reviews in Eguiarte et al, 2013 , 2021 ; Klimova et al, 2022 ), a pattern that is maintained in part by the most important agave pollinators, such as the nectarivorous bats, Leptonycteris nivalis and L. yerbabuenae ( Eguiarte, Souza & Silva-Montellano, 2000 ; Rocha et al, 2006 ; Trejo-Salazar, Scheinvar & Eguiarte, 2015 ; Eguiarte et al, 2021 ). Recent conservation and management initiatives have focused on preserving the natural agave pollinators ( e.g ., bats) and, at the same time, mitigating genomic erosion and promoting sustainable practices of the agroecosystems where the main crop is agave used for mezcal, tequila, and other agave distillates production ( Trejo-Salazar et al, 2016 ; see also ).…”

“…The recent advent of reduced representation genomic strategies that allows the analysis of many individuals and thousands of single nucleotide polymorphisms (SNPs) has revolutionized studies on the genetic diversity in plant and animal species ( Barrera-Redondo, Piñero & Eguiarte, 2020 ; Eguiarte et al, 2022 ). This type of markers allows to perform a more precise analysis of the micro-evolutionary processes that occur in the species and the exploration of diversity throughout the entire genome and was recently successfully used in a close relative of A. tequilana, A. angustifolia ( Cabrera-Toledo et al, 2020 ; Klimova et al, 2022 ). We believe that information on genome-wide patterns of genetic variation and knowledge of the population structure of A. tequilana will be essential in defining management priorities, developing new sustainable cropping systems, and understanding the impact of domestication on its genetic repertoire.…”