Unraveling the complex hybrid ancestry and domestication history of cultivated strawberry

Authors: Hardigan, Michael; LORANT, ANNE - University Of California, Davis; PINCOT, DOMINIQUE - University Of California, Davis; FELDMANN, MITCHELL - University Of California, Davis; FAMULA, RANDI - University Of California, Davis; ACHARYA, CHARLOTTE - University Of California, Davis; LEE, SEONGHEE - University Of Florida; VERMA, SUJEET - University Of Florida; WHITAKER, VANCE - University Of Florida; Bassil, Nahla; Zurn, Jason; COLE, GLENN - University Of California, Davis; BIRD, KEVIN - Michigan State University; EDGER, PATRICK - Michigan State University; KNAPP, STEVEN - University Of California, Davis

Submitted to: Molecular Biology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/4/2021
Publication Date: 1/28/2021
Citation: Hardigan, M.A., Lorant, A., Pincot, D., Feldmann, M., Famula, R., Acharya, C., Lee, S., Verma, S., Whitaker, V., Bassil, N.V., Zurn, J.D., Cole, G., Bird, K., Edger, P., Knapp, S. 2021. Unraveling the complex hybrid ancestry and domestication history of cultivated strawberry. Molecular Biology and Evolution. 38(6):2285-2305. https://doi.org/10.1093/molbev/msab024.
DOI: https://doi.org/10.1093/molbev/msab024

Interpretive Summary: The domestication histories of cultivated plant species carry important lessons for modern breeders; their exploration can tell us how adaptation to agriculture influenced genetic diversity, population structure, and wild conservation. The effects of historic selection and genetic bottlenecks are etched into the genomes of modern individuals. The popular horticultural crop “garden strawberry” is an octoploid hybrid with a unique domestication history tracing back only 300 years. There are few examples of species domesticated so quickly and recently, while operating on genetic diversity from two wild gene pools. Exploring strawberry domestication in a genomic context is useful for applied breeders who wish to understand the landscape of diversity and its preservation, as well as basic researchers interested in alternative domestication models, or understanding how genetic diversity from two wild species coexists in a crop hybrid complex. In-depth studies of strawberry domestication from a genetic perspective were impossible until recently, due to the complexity of the octoploid genome and inability to resolve subgenome-level DNA variation. This study used an octoploid reference genome and 1,537 octoploid individuals genotyped by sequencing or DNA marker arrays to investigate strawberry genetic diversity, ancestral allele retention, population structure, and selective sweeps. This study provides a roadmap for the breeding community to understand strawberry diversity and structure, and the impacts of selection on an important horticultural fruit crop.

Technical Abstract: Cultivated strawberry (Fragaria × ananassa) is one of our youngest domesticates, originating in early eighteenth century Europe from spontaneous hybrids between wild allo-octoploid species (F. chiloensis and F. virginiana). Several agriculturally important phenotypes have been improved by breeding over the last 300 years, thereby enabling the global expansion of strawberry production. Here, we describe the genomic history of strawberry domestication from the earliest hybrids to modern cultivars. We observed a significant increase in heterozygosity among interspecific hybrids and a decrease in heterozygosity among domesticated descendants of those hybrids. Selective sweeps were found across the genome in early and modern phases of domestication - 59-76% of the selectively swept genes originated in the three less dominant ancestral subgenomes. Contrary to the tenet that genetic diversity is limited in cultivated strawberry, we found that the octoploid species harbor massive allelic diversity and that F. × ananassa harbors as much allelic diversity as either wild founder. We identified 41.8M subgenome-specific DNA variants among resequenced wild and domesticated individuals. Strikingly, 98% of common alleles and 73% of total alleles were shared between wild and domesticated populations. Moreover, genome-wide estimates of nucleotide diversity were virtually identical in F. chiloensis, F. virginiana, and Fragaria × ananassa (pi = 0.0059-0.0060). We found, however, that nucleotide diversity and heterozygosity were significantly lower in modern Fragaria × ananassa populations that have experienced significant genetic gains and been the source of numerous agriculturally important cultivars.