Maintenance and expansion of genetic and trait variation following domestication in a clonal crop

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  • Oliver W. White
    Royal Botanic Gardens, Kew
  • Manosh Kumar Biswas
    University of Leicester
  • Wendawek M. Abebe
    Hawassa University, Ethiopia
  • Yann Dussert
    Université de Poitiers, CESCM
  • Firew Kadebe
    Hawassa University, Ethiopia
  • Richard A. Nichols
    Queen Mary University of London
  • Richard J.A. Buggs
    Royal Botanic Gardens, Kew
  • Sabsebe Demissew
    Addis Ababa University
  • Feleke Woldeyes
    Ethiopian Biodiversity Institute, Addis Ababa, Ethiopia
  • Alexander S. T. Papadopulos
  • Trude Schwarzacher
    University of Leicester
  • Pat J.S. Heslop-Harrison
    University of Leicester
  • Paul Wilkin
    Royal Botanic Gardens, Kew
  • James S. Borrell
    Royal Botanic Gardens, Kew
Clonal propagation enables favourable crop genotypes to be rapidly selected and multiplied. However, the absence of sexual propagation can lead to low genetic diversity and accumulation of deleterious mutations, which may eventually render crops less resilient to pathogens or environmental change. To better understand this trade-off, we characterize the domestication and contemporary genetic diversity of Enset (Ensete ventricosum), an indigenous African relative of bananas (Musa) and a principal starch staple for 20 million Ethiopians. Wild enset reproduction occurs strictly by sexual outcrossing, but for cultivation, it is propagated clonally and associated with diversification and specialization into hundreds of named landraces. We applied tGBS sequencing to generate genome-wide genotypes for 192 accessions from across enset's cultivated distribution, and surveyed 1340 farmers on enset agronomic traits. Overall, reduced heterozygosity in the domesticated lineage was consistent with a domestication bottleneck that retained 37% of wild diversity. However, an excess of putatively deleterious missense mutations at low frequency present as heterozygotes suggested an accumulation of mutational load in clonal domesticated lineages. Our evidence indicates that the major domesticated lineages initially arose through historic sexual recombination associated with a domestication bottleneck, followed by the amplification of favourable genotypes through an extended period of clonal propagation. Among domesticated lineages, we found a significant phylogenetic signal for multiple farmer-identified food, nutrition and disease resistance traits and little evidence of contemporary recombination. The development of future-climate adapted genotypes may require crop breeding, but outcrossing risks exposing deleterious alleles as homozygotes. This trade-off may partly explain the ubiquity and persistence of clonal propagation over recent centuries of comparative climate stability.
Original languageEnglish
Pages (from-to)4165-4180
JournalMolecular Ecology
Volume32
Issue number15
Early online date2 Jun 2023
DOIs
Publication statusPublished - Aug 2023

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