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DOMESTICATION HISTORY of STRAWBERRY: SELECTION and BOTTLENECKS SHAPING the OCTOPLOID HYBRID COMPLEX Michael A

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DOMESTICATION HISTORY of STRAWBERRY: SELECTION and BOTTLENECKS SHAPING the OCTOPLOID HYBRID COMPLEX Michael A DOMESTICATION HISTORY OF STRAWBERRY: SELECTION AND BOTTLENECKS SHAPING THE OCTOPLOID HYBRID COMPLEX Michael A. Hardigan1, Thomas J. Poorten1, Charlotte Acharya1, Glenn S. Cole1, National Institute of Kim E. Hummer2, Nahla Bassil2, Patrick Edger3, and Steven J. Knapp1 Food and Agriculture 1Department of Plant Sciences, University of California Davis, Davis CA 95616; 2USDA-ARS, National Clonal Germplasm Repository, Corvallis OR 97333; Department of Horticulture, Michigan State University, East Lansing MI 48824 Background Domesticated strawberry (Fragaria x ananassa) is an octoploid hybrid (2n=8x=56) of Chilean beach strawberry (F. chiloensis [L.] Miller) and North American common strawberry (F. virginiana Genetic Restructuring Effects of Day-Neutral Strawberry Breeding Miller) originating in the mid-18th century. Subsequent breeding established elite genetic STRUCTURE analysis revealed strawberry genetics were restructuring over time along lines of architectures of F. x ananassa. Hybrids developed at the University of California represent a maturity phenotype as a result of selection of photoperiod-insensitive flowering at UC, with unique modern group, accounting for 60% of worldwide consumption. To explore key events distinct groups having increasing day neutrality since 1980s. underlying the emergence of globally important strawberry populations, we studied the impacts of selection, population bottlenecks, and migration on restructuring of genetic diversity within A the F. x ananassa hybrid complex using a panel of 1,300 elite and wild octoploid Fragaria UC_Ananassa_genetics_-_subgroup_1Fragaria_chiloensis UC_Ananassa_genetics_-_subgroup_2 UC_Ananassa_genetics_-_subgroup_3 UC_Ananassa_genetics_-_subgroup_4nonUC_&_early_1900s_UC_Ananassa,_Fragaria_virginiana genotypes. The panel was genotyped with 16,492 subgenome-specific single nucleotide polymorphisms anchored to an improved diploid reference assembly. We show that significant restructuring of the hybrid complex followed domestication, including historic selection favoring the North American wild progenitor genome, and a 20th century bottleneck separating UC genotypes from octoploids bred elsewhere in North America and Europe. Greater divergence was uncovered between modern UC and non-UC F. x ananassa (FST=0.207) than non-UC cultivars and their wild progenitors (FST=0.182). This bottleneck exploited post-domestication subspecific introgressions that redirected selection toward the South American genome and photoperiod- B C Flowering Phenotype insensitive flowering from a high-elevation ecotype of F. virginiana subsp. glauca, causing a Germplasm % day Group % UC % Cv. Group 6 dayDay−-neutralneutral transition from complex polygenic day-neutrality to QTL regions on a single chromosome arm, Composition neutral shortShort−-dayday independent of the TERMINAL FLOWERING1 source discovered in diploid ancestor Fragaria vesca. 1 UC germplasm 99.5 12.7 25.4 Group 5 FloweringunknownUnknown We report that strawberry breeding targeted genes controlling hormone-mediated fruit F. chiloensis (N.A. Phenotype 2 4.2 0.0 NA expansion, and expression pathways within developing achenes. + S.A.) day−neutral STRUCTURE Cluster STRUCTURE Group 4 3 UC germplasm 99.7 4.1 11.0 short−day unknown Genetic Relationships of Octoploid Fragaria 4 UC germplasm 100.0 3.0 34.7 Group 3 Phylogenetic lineages of octoploid strawberry germplasm. Clear separation of University of 5 UC germplasm 100.0 1.4 56.7 Cluster STRUCTURE California F. x ananassa from non-UC F. x ananassa revealed west coast strawberry to be Group 1 F. virginiana + genetically distinct from their progenitors. 6 5.3 Group82.0 13456 5.2 non-UC ananassa 1900 19001950 1950 2000 2000 1950 2011 Taxa Year Year Year F. chiloensis Figure 3. Temporal structuring of strawberry genetics as related to selection for day-neutral flowering trait. (A) Population structure of octoploid strawberry diversity panel. (B) Descriptions and rates of UC SD DN F. virginiana strawberry genetics, day-neutral flowering within each population group. (C) Plot of release year and Flowering non-UC F. x ananassamaturity phenotype for cultivated population groups. Taxa UC F.Distinct x ananassaGenetic Mechanisms of Day-Neutral Flowering F. chiloensis 1950 Parallel2011 GWAS and analysis of selective sweeps in short-day versus day-neutral octoploids uncovered a 1.5 F. virginiana transitionYear from polygenic additive mechanisms in historic germplasm to simpler genetic control by QTLs on 1.5 a single chromosome arm in modern day-neutral genotypes. non-UC F. x ananassa SD DN 1.0 FST UC F. x ananassa Flowering 1.0 FST A Day-Neutralpre−1990 – Pre1990 Day-NeutralUC−last – decadeLast Decade B .5 0.50 Fvb1 0.5 Fvb1 0.5 Selection Test 0.25.25 15 Selection Test 0.000 val) wild Fragaria/non−UC ananassa − .5 value) 0.0 0.50 Fvb2 - 0.0 wild Fragaria/non−UC ananassa Fvb2 10 non−UC ananassa/UC ananassa − post2000 0.25.25 non−UC ananassa/UC ananassa − post2000 0.000 1.5 non−UC ananassa/UC ananassa − pre1970 log10(p 5 − .5 log10(p 0.50 Fvb3 1.5 - non−UC ananassa/UC ananassa − pre1970 Fvb3 0.25.25 nucdiv Observation Density 0 nucdiv FST Observation Density 1.0 FST 1.0 0.000 1.5 .5 0.40.4 0.50 Fvb4 1.5 Fvb4 Position 0.30.3 1.5 .25 Position 0.25FST 0.5 1.5 0.20.2 FST 0.5 1.0 0.000 0.1 C 1.51.0 FST FST Estimate FST .5 FST 0.50 Fvb5 0.0 1.01.5 Fvb5 40 0.0 FST 1.5 1.0 1.5 0.25.25 0.0 0.5 Figure 1. 1.5Phylogenetic tree of strawberry octoploids – F. chiloensis (orange), nonFST = test -UC F. FST −1 0 1 FST = test 30 1.00.5 0.000 val) FST x ananassaSelection(green), Test F. virginiana (blue), and University of California F. x ananassa −1 0 1 − 0.51.0 0.50.5 value) - FST Selected Allele − Fvb6 0.5 (turquoise). Red clades indicate polytomy. Exterior Selection1.0 Test heatmaps indicate release year Fvb6 Selected Allele − PopulationSelectionwild1.0 Fragaria/non Test Selection−UC ananassa Analysis FST 20 Hybrid Progenitor Frequency0.0 Balance Population1.0 Selection Analysis 0.25.25 Hybrid Progenitor Frequency0.50.0 Balance (layer 1) and maturity phenotype (layer 2; green = day neutral, white = short day).Selectionwild Fragaria/non Test −UC ananassa wild Fragaria/non Fragaria à−UChistoric/non ananassa -UC ananassa 0 0.00.5 Selectionnon−UC Test ananassa/UC ananassa − post2000 0.00 log10(p wild Fragaria/non Fragaria à−UChistoric/non ananassa -UC ananassa − 0.0 non−UC ananassa/UC ananassa − post2000 0.50.5 log10(p 10 Fvb7 Selection Test - 1.5 Fvb7 1.5 Selectionwildnonhistoric/non0.51.5− Fragaria/nonUCof ananassa/UCDistinct-UC−UC ananassaHybrid ananassa ananassaAncestralà − pre1970post2000UC ananassaGenomes– pre-1970 0.0 1.5 FST = test .25 1.5 wildnonhistoric/non0.5− Fragaria/nonUC ananassa/UC-UC−UC ananassa ananassa ananassaà − pre1970post2000UC ananassa – pre-1970 0.25 1.50.0 F. x ananassanon−UC ananassa/UCbreeding at ananassathe University − pre1970 of California redirected selectionFST = test Selection Test 0 non−UC ananassa/UC ananassa − post2000 0 nucdiv historic/non-UC ananassa à UC ananassa – post-2000 Selection0.00 Test Observation Density 1.5 non−UC ananassa/UC ananassa − pre1970 non−UC ananassa/UC ananassa − post2000 FST 0 5 1010 1515 2020 2525 3030 3535 0 5 1010 1515 2020 2525 3030 3535 nucdiv historic/non-UC ananassa à UC ananassa – post-2000 Observation Density 1.0 from the1.0F. virginiana ancestor toward South American F. chiloensis. wild Fragaria/non−UC ananassa Position 1.0 FST Position (Mb) nucdiv 0.0 Observation Density 1.51.0 non0.01.0−UC ananassa/UC ananassa − pre1970 wild Fragaria/non−UC ananassaPosition (Mb) Position nucdiv 0.0 Observation Density 1.01.5 non0.0−UC ananassa/UC ananassa − pre1970 1.0 nonFigure 4. −UC Selective sweeps and GWAS results for dayananassa/UC ananassa − post2000 -neutral flowering trait (A) Genome-wide view of allele fixation nucdiv Observation Density 0.5 non−UC ananassa/UC ananassa − post2000 nucdiv Observation Density 1.00.5 0.5 (FST) comparing short-day strawberry to pre-1990 and post-2000 day-neutral types. (B) Manhattan plot of pre-1990 0.51.0 1.50.5 Non-UC UC (post-2000) non−UC ananassa/UC ananassa − pre1970 1.5 = test nonday-−neutral flowering GWAS. (C) Manhattan plot of postUC ananassa/UC ananassa − pre1970 -2000 day-neutral flowering GWAS. 0.5 1.5 FST = test Selection Test selected = test 0.0 selected alleles FST = test Selection Test 0.5 0.0 nucdiv Observation Density alleles wild Fragaria/non−UC ananassa −1 0 1 FST 0.5 Density Observation 0.0 0.0 0.0 nucdiv UC Strawberry Bottleneck Observation Density 1.0 wild Fragaria/non−UC ananassa −1 0 1 1.0 FST Observation Density Observation 0.0 0.0 0.0 p −1 Selected0 Allele − 1 1.0 Marker nucleotide diversity and allele fixation (F ) of wild and cultivated groups indicated bottlenecking of UC p non−UC ananassa/UC ananassa − post2000 ST 0.0 −1 Hybrid ProgenitorSelected Frequency0 Allele − Balance 1 ratio non−UC ananassa/UC ananassa − post2000 0.0 Selected Allele − ratio diversity over time, accompanied by increased selective pressure impacting a large percentage of SNP loci. −1 Hybrid ProgenitorSelected 0Frequency Allele − Balance 1 Hybrid Progenitor Frequency Balance 0.51.5 non−UC ananassa/UC ananassa − pre1970 0.5 = test −1 Hybrid ProgenitorSelected Frequency0 Allele − Balance 1 0.51.5 non−UC ananassa/UC ananassa − pre1970 0.5 = test Selected Allele − Selection0.5 Test 1.00 Figure 5. Metrics revealing Hybrid Progenitor Frequency Balance nucdiv Observation Density Selection Test increased selective pressure Observation Density Observation Hybrid Progenitor Frequency Balance nucdiv Observation Density 1.0 wild Fragaria/non−UC ananassa Observation Density Observation 0.0 p 0.4 within the UC strawberry 1.0 wild Fragaria/non−UC ananassa 0.75 0.0 p −1 0 1 ratio non−UC ananassa/UC ananassa − post2000 breeding program, including −1 0 1 ratio −1 0 1 non0.3−UC ananassa/UC ananassa − post2000 marker nucleotide diversity (π) 0.5F.
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