Genome-wide genotyping elucidates the geographical diversification and dispersal of the polyploid and clonally propagated yam (Dioscorea alata).

Dioscorea alata Clonal propagation demography geographical distribution polyploidy population genomics yam

Journal

Annals of botany
ISSN: 1095-8290
Titre abrégé: Ann Bot
Pays: England
ID NLM: 0372347

Informations de publication

Date de publication:
30 10 2020
Historique:
received: 18 03 2020
accepted: 22 06 2020
pubmed: 28 6 2020
medline: 2 12 2020
entrez: 28 6 2020
Statut: ppublish

Résumé

Inferring the diffusion history of many human-dispersed species is still not straightforward due to unresolved past human migrations. The centre of diversification and routes of migration of the autopolyploid and clonally propagated greater yam, Dioscorea alata, one of the oldest edible tubers, remain unclear. Here, we address yam demographic and dispersal history using a worldwide sample. We characterized genome-wide patterns of genetic variation using genotyping by sequencing 643 greater yam accessions spanning four continents. First, we disentangled the polyploid and clonal components of yam diversity using allele frequency distribution and identity by descent approaches. We then addressed yam geographical origin and diffusion history with a model-based coalescent inferential approach. Diploid genotypes were more frequent than triploids and tetraploids worldwide. Genetic diversity was generally low and clonality appeared to be a main factor of diversification. The most likely evolutionary scenario supported an early divergence of mainland Southeast Asian and Pacific gene pools with continuous migration between them. The genetic make-up of triploids and tetraploids suggests that they have originated from these two regions before westward yam migration. The Indian Peninsula gene pool gave origin to the African gene pool, which was later introduced to the Caribbean region. Our results are congruent with the hypothesis of independent domestication origins of the two main Asian and Pacific gene pools. The low genetic diversity and high clonality observed suggest a strong domestication bottleneck followed by thousands of years of widespread vegetative propagation and polyploidization. Both processes reduced the extent of diversity available for breeding, and this is likely to threaten future adaptation.

Sections du résumé

BACKGROUND AND AIMS
Inferring the diffusion history of many human-dispersed species is still not straightforward due to unresolved past human migrations. The centre of diversification and routes of migration of the autopolyploid and clonally propagated greater yam, Dioscorea alata, one of the oldest edible tubers, remain unclear. Here, we address yam demographic and dispersal history using a worldwide sample.
METHODS
We characterized genome-wide patterns of genetic variation using genotyping by sequencing 643 greater yam accessions spanning four continents. First, we disentangled the polyploid and clonal components of yam diversity using allele frequency distribution and identity by descent approaches. We then addressed yam geographical origin and diffusion history with a model-based coalescent inferential approach.
KEY RESULTS
Diploid genotypes were more frequent than triploids and tetraploids worldwide. Genetic diversity was generally low and clonality appeared to be a main factor of diversification. The most likely evolutionary scenario supported an early divergence of mainland Southeast Asian and Pacific gene pools with continuous migration between them. The genetic make-up of triploids and tetraploids suggests that they have originated from these two regions before westward yam migration. The Indian Peninsula gene pool gave origin to the African gene pool, which was later introduced to the Caribbean region.
CONCLUSIONS
Our results are congruent with the hypothesis of independent domestication origins of the two main Asian and Pacific gene pools. The low genetic diversity and high clonality observed suggest a strong domestication bottleneck followed by thousands of years of widespread vegetative propagation and polyploidization. Both processes reduced the extent of diversity available for breeding, and this is likely to threaten future adaptation.

Identifiants

pubmed: 32592585
pii: 5864103
doi: 10.1093/aob/mcaa122
pmc: PMC7596366
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1029-1038

Informations de copyright

© The Author(s) 2020. Published by Oxford University Press on behalf of the Annals of Botany Company.

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Auteurs

Bilal Muhammad Sharif (BM)

CIRAD, UMR AGAP, F34398-Montpellier, France.
AGAP, Univ Montpellier, CIRAD, INRA, Montpellier SupAgro, Montpellier, France.
University of Vienna, Department of Evolutionary Anthropology, Vienna, Austria.

Concetta Burgarella (C)

CIRAD, UMR AGAP, F34398-Montpellier, France.
AGAP, Univ Montpellier, CIRAD, INRA, Montpellier SupAgro, Montpellier, France.
Uppsala University, Department of Organismal Biology, Uppsala, Sweden.

Fabien Cormier (F)

AGAP, Univ Montpellier, CIRAD, INRA, Montpellier SupAgro, Montpellier, France.
CIRAD, UMR AGAP, Petit Bourg, Guadeloupe, France.

Pierre Mournet (P)

CIRAD, UMR AGAP, F34398-Montpellier, France.
AGAP, Univ Montpellier, CIRAD, INRA, Montpellier SupAgro, Montpellier, France.

Sandrine Causse (S)

CIRAD, UMR AGAP, F34398-Montpellier, France.
AGAP, Univ Montpellier, CIRAD, INRA, Montpellier SupAgro, Montpellier, France.

Kien Nguyen Van (KN)

Plant Resources Center (PRC), An Khanh, Hoai Duc, Hanoi, Vietnam.

Juliane Kaoh (J)

Vanuatu Agricultural Research and Technical Centre (VARTC), Espiritu Santo PB, Vanuatu.

Mamy Tiana Rajaonah (MT)

Kew Madagascar Conservation Centre, Antananarivo, Madagascar.

Senanayake Ravinda Lakshan (SR)

Field Crops Research and Development Institute (FCRDI), Mahailluppallama, Anuradhapura, Sri Lanka.

Jeffrey Waki (J)

National Agricultural Research Institute (NARI), Lae, Morobe Province, Papua New Guinea.

Ranjana Bhattacharjee (R)

International Institute of Tropical Agriculture (IITA), PMB, Ibadan, Oyo State, Nigeria.

Gueye Badara (G)

International Institute of Tropical Agriculture (IITA), PMB, Ibadan, Oyo State, Nigeria.

Babil Pachakkil (B)

Tokyo University of Agriculture (TUA), Sakuragaoka, Setagaya-ku, Tokyo, Japan.

Gemma Arnau (G)

AGAP, Univ Montpellier, CIRAD, INRA, Montpellier SupAgro, Montpellier, France.
CIRAD, UMR AGAP, Petit Bourg, Guadeloupe, France.

Hana Chaïr (H)

CIRAD, UMR AGAP, F34398-Montpellier, France.
AGAP, Univ Montpellier, CIRAD, INRA, Montpellier SupAgro, Montpellier, France.

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