Pleistocene-dated genomic divergence of avocado trees supports cryptic diversity in the Colombian germplasm

Abstract Genomic characterization of ex situ plant collections optimizes the utilization of genetic resources by identifying redundancies among accessions, capturing cryptic variation, establishing reference collections, and ultimately assisting pre-breeding and breeding efforts. Yet, the integration of evolutionary genomic analyses is often lacking when studying the biodiversity of crop gene pools. Such is the case in the avocado, Persea americana Mill., an iconic American fruit tree crop that has seen an unprecedented expansion worldwide because of its nutritional properties. However, given a very restricted number of commercial clones, avocado plantations are becoming more vulnerable to diseases and climate change. Therefore, exploring new sources of evolutionary novelty and genetic diversity beyond the commercial varieties derived from traditional genetic pools in Mexico and Central America is imperative. To fill this gap, we aimed to characterize the genomic diversity of Colombian avocado trees. Specifically, we constructed reduced representation genomic libraries to genotype by sequencing 144 accessions from the Colombian National genebank and 240 materials from local commercial orchards in the Colombian northwest Andes. We merged the resulting reads with available sequences of reference genotypes from known avocado groups (also named as races), Mexican, Guatemalan, and West Indian, to discover 4931 SNPs. We then analyzed the population structure and phylogenetic diversity, and reconstructed evolutionary scenarios, possibly leading to new genetic groups in Colombian germplasm. We detected demographic stratification despite evidence of intergroup gene flow. Besides the classical three avocado groups, we found an exclusive Colombian group with a possible genetic substructure related to the geographical origin (Andean and Caribbean). Phylogenetic and ABC demographic modeling suggested that the Colombian group evolved in the Pleistocene before human agriculture started, and its closest relative from the three recognized races would be the West Indian group. We conclude that northwest South America offers a cryptic source of allelic novelty capable of boosting avocado pre-breeding strategies to select rootstock candidates well adapted to specific eco-geographical regions in Colombia and abroad.