Genetic diversity and population structure show different patterns of diffusion for bitter and sweet manioc in Brazil

Genetic Resources and Crop Evolution volume 66, pages1773–1790(2019)Cite this article

Abstract

Although many important crops originated in Amazonia, the general patterns of their evolutionary histories are still obscure. Currently a major global food crop, manioc originated in southwestern Amazonia and was dispersed throughout the lowland Neotropics before the European conquest. However, little is known about the origin of the bitter and sweet landraces, nor the routes by which these were dispersed in Brazil and beyond. We used a non-systematic Brazil-wide sample of 494 manioc landraces from 11 geographic regions, and ten nuclear microsatellite markers to analyze the genetic diversity of sweet and bitter manioc. Bayesian simulations highlighted the bitter–sweet divergence and also suggested the existence of two groups of sweet manioc (circum-Cerrado and general Brazil) and two groups of bitter manioc (upper Negro River and general Brazil), while the relationships among geographic regions were depicted with clustering analysis. Overall we suggest that: (1) manioc was initially domesticated to be sweet, was then dispersed from southwestern Amazonia into both the Amazon basin and the Cerrado; (2) that bitter manioc arose from the general Brazilian sweet manioc landraces, almost certainly in Amazonia, where bitter manioc became most important and was dispersed both throughout Amazonia and along the Brazilian coast, but especially to the upper Negro River, where it became most diverse. Our study adds insights to the knowledge about how native Amazonian crops have been managed across their history of domestication.

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Data availability statement

The majority of the data set, with passport information and full microsatellite allele data has been uploaded in Online Resource 1 Supplementary Table S1. The indigenous manioc landraces collected by the Bilateral Project CNPq/Instituto Socioambiental—ISA/Institut de Recherche pour le Développement—IRD, proc. No. 91.0211/97-3, are not included, since these require separate authorization from the Federação das Organizações Indígenas do Rio Negro—FOIRN. Please contact GSM for guidance to obtain this new authorization.

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Acknowledgements

The authors thank the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, 00/00239-3 and 00/00240-1), for primary funding, the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, CT-Amazônia-575588/08-0) for logistic and analytical support, the numerous traditional and indigenous farmers who agreed to our collections, the Bilateral Project CNPq/Instituto Socioambiental (ISA)/Institut de Recherche pour le Développement (IRD), (CNPq, 91.0211/97-3). We thank the French Bureau des Ressources Génétiques, for use of manioc landraces from the upper Negro River, ISA and the Federação das Organizações Indígenas do Rio Negro (FOIRN) for authorizing reuse of the genetic information from the manioc landraces of the upper Negro River. We thank Laure Emperaire (IRD), Doyle McKey (Université de Montpellier), Manuel Arroyo-Kalin (University College London), for comments on the manuscript, and Josefino Fialho (Embrapa Cerrados), for several manioc samples. AA-P thanks Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, 51/2013) and FAPESP (2018/00036-9) for post-doctoral scholarships. CRC thanks CNPq (303851/2015-5) for a research fellowship.

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Affiliations

  1. Universidade Federal de Rondônia, Av. Norte-Sul, 7300, Rolim de Moura, Rondônia, 76940-000, Brazil

    Gilda Santos Mühlen

  2. Laboratório de Evolução Aplicada, Universidade Federal do Amazonas, Manaus, Amazonas, 69077-000, Brazil

    Gilda Santos Mühlen, Alessandro Alves-Pereira & Charles R. Clement

  3. Laboratório de Análise Genética e Molecular, Centro de Biologia Molecular e Engenharia Genética, Departamento de Biologia Vegetal, Instituto de Biologia, Universidade Estadual de Campinas, Av. Cândido Rondon, 400, Caixa Postal: 6010, Campinas, São Paulo, 13083-875, Brazil

    Alessandro Alves-Pereira

  4. Instituto Agronômico de Campinas, Av. Barão de Itapura 1481, Campinas, São Paulo, 13012-970, Brazil

    Cássia Regina Limonta Carvalho & Teresa Losada Valle

  5. Instituto Nacional de Pesquisas da Amazônia – INPA, Av. André Araújo, 2936, Manaus, Amazonas, 69067-375, Brazil

    André Braga Junqueira & Charles R. Clement

  6. Institut de Ciència i Tecnologia Ambientals, Universitat Autònoma de Barcelona, 08193, Bellaterra, Barcelona, Spain

    André Braga Junqueira

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  1. Gilda Santos Mühlen
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Contributions

GSM and TLV designed research, GSM, TLV and CRLC performed research, GSM, TLV and CRLC contributed reagents, GSM, AA-P and CRC analyzed data, ABJ contributed GIS support and map design, GSM, AA-P, CRC, TLV, and ABJ wrote the paper.

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Correspondence to Alessandro Alves-Pereira.

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Supplementary Table S1

Passport data, SSR genotypes and ancestry coefficients of Structure analysis for 494 Brazilian manioc landraces. Supplementary Table S2 Microsatellite identification, size range in base pairs (bp), number of alleles (A), observed heterozygosity (HO), expected heterozygosity (HE), and inbreeding coefficient (f) estimated from 494 Brazilian manioc landraces. Loci were developed by aChavarriaga-Aguirre et al. (1998) and bMba et al. (2001). *significant at p < 0.05 (XLSX 119 kb)

Supplementary Fig. S1

Plot of ΔK of possible groups of 494 Brazilian manioc landraces obtained from ten Structure analysis simulations. The Structure analysis was extended to K = 20 because of the 11 geographical groupings of the manioc landraces, nine of which had both bitter and sweet manioc. Supplementary Fig. S2 Comparison of principal coordinate analyses according to different groupings of the 494 Brazilian manioc landraces screened with ten SSR loci. Groups according to A) bitter and sweet identification by passport data, and according to results of Structure analysis for B) K = 2, C) K = 3 and D) K = 4. Supplementary Fig. S3 Proportional representation of the four major groups of Brazilian manioc landraces identified by the Structure analysis within the 11 geographically-defined groupings (DOC 1967 kb)

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Mühlen, G.S., Alves-Pereira, A., Carvalho, C.R.L. et al. Genetic diversity and population structure show different patterns of diffusion for bitter and sweet manioc in Brazil. Genet Resour Crop Evol 66, 1773–1790 (2019). https://doi.org/10.1007/s10722-019-00842-1

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Keywords

  • Bayesian clustering
  • Cassava
  • Domestication
  • Genetic relationships
  • Geographic distribution
  • Manihot esculenta