Wide Hybrids Uncover Useful Heterosis, Good Inbreeding, and Outbreeding Depression in Strawberry

Authors: FELDMANN, MITCHELL - University Of California, Davis; PINCOT, DOMINIQUE - University Of California, Davis; Hardigan, Michael; SEYMOUR, DANELLE - University Of California, Riverside; FAMULA, RANDI - University Of California, Davis; LÓPEZ, CINDY - University Of California, Davis; BJORNSON, MARTA - University Of California, Davis; JIMENEZ, NICOLAS - University Of California, Davis; PETRASCH, STEFAN - Rijk Zwaan Breeding Bv; BLANCO-ULATE, BARBARA - University Of California, Davis; COLE, GLENN - University Of California, Davis; KNAPP, STEVEN - University Of California, Davis

Submitted to: Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/16/2024
Publication Date: 2/29/2024
Citation: Feldmann, M.J., Pincot, D.D., Hardigan, M.A., Seymour, D.K., Famula, R., López, C.M., Bjornson, M., Jimenez, N.P., Petrasch, S., Blanco-Ulate, B., Cole, G.S., Knapp, S.J. 2024. Wide Hybrids Uncover Useful Heterosis, Good Inbreeding, and Outbreeding Depression in Strawberry. Genetics.

Interpretive Summary: The increased vigor and productivity of between-species hybrids has played a critical role in the domestication of strawberry and global expansion of strawberry production. This fascinating plant carries four ancestral genomes that are each functionally equivalent to the entire genomes found in many plants, humans, and domesticated animals. Our study delved into genetic mysteries surrounding hybrid vigor and the impact of population bottlenecks and a century of breeding on genetic diversity in strawberry.

Technical Abstract: The domestication of strawberry (Fragaria × ananassa), an artificial homoploid hybrid species, was driven by interspecific (between-group) heterosis and perhaps by progressive (inter-subgenomic) heterosis, a phenomenon hypothesized to be important in polyploids. Within-population breeding schemes have historically been applied in strawberry hybrid development without exploiting heterotic patterns. Here we show that hybrids developed within an elite, bottlenecked population (the ‘California’ population) are high yielding despite being 54-79% inbred. That population was found to lack a discernible group structure. We discovered that heterosis was limited or non-existent for fruit yield and quality traits among elite × elite California population hybrids. Strikingly, heterosis estimates were either not different from zero or negative for fruit yield among 98.8% of those hybrids. Heterosis was positive for 28.0-60.6% of elite × exotic hybrids for fruit quality traits, compared to 1.4-4.3% for fruit yield, weight, or firmness. Heterosis appears to have decayed in the California population, which we attributed to increased inbreeding caused by the accumulation of favorable incompletely to completely dominant alleles for traits under selection, genetic drift, and selective sweeps. We found that the highest yielding strawberry hybrids reported to date are among the most highly inbred, which seems counterintuitive, especially for a highly heterozygous, outbreeding hybrid species harboring heavy genetic loads. Despite breeding-associated within-population genetic erosion, the genomes of high yielding hybrids appear to be heterozygous (segregating) for 20,370-49,680 of the 97,000-108,000 genes annotated in octoploid genome assemblies, the equivalent of an entire diploid genome or more.