Divergent evolutionary and epidemiological dynamics of cassava mosaic geminiviruses in Madagascar.
Cassava mosaic disease (CMD) in Madagascar is caused by a complex of at least six African cassava mosaic geminivirus (CMG) species. This provides a rare opportunity for a comparative study of the evolutionary and epidemiological dynamics of distinct pathogenic crop-infecting viral species that coexist within the same environment. The genetic and spatial structure of CMG populations in Madagascar was studied and Bayesian phylogeographic modelling was applied to infer the origins of Madagascan CMG populations within the epidemiological context of related populations situated on mainland Africa and other south western Indian Ocean (SWIO) islands.



The isolation and analysis of 279 DNA-A and 117 DNA-B sequences revealed the presence in Madagascar of four prevalent CMG species (South African cassava mosaic virus, SACMV; African cassava mosaic virus, ACMV; East African cassava mosaic Kenya virus, EACMKV; and East African cassava mosaic Cameroon virus, EACMCV), and of numerous CMG recombinants that have, to date, only ever been detected on this island. SACMV and ACMV, the two most prevalent viruses, displayed low degrees of genetic diversity and have most likely been introduced to the island only once. By contrast, EACMV-like CMG populations (consisting of East African cassava mosaic virus, EAMCKV, EACMCV and complex recombinants of these) were more diverse, more spatially structured, and displayed evidence of at least three independent introductions from mainland Africa. Although there were no statistically supported virus movement events between Madagascar and the other SWIO islands, at least one mainland African ACMV variant likely originated in Madagascar.



Our study highlights both the complexity of CMD in Madagascar, and the distinct evolutionary and spatial dynamics of the different viral species that collectively are associated with this disease. Given that more distinct CMG species and recombinants have been found in Madagascar than any other similarly sized region of the world, the risks of recombinant CMG variants emerging on this island are likely to be higher than elsewhere. Evidence of an epidemiological link between Madagascan and mainland African CMGs suggests that the consequences of such emergence events could reach far beyond the shores of this island.
CIRAD, UMR PVBMT, Pôle de Protection des Plantes, 7 chemin de l'IRAT, Saint-Pierre, Ile de la Réunion, 97410, France.|Université de la Réunion, UMR PVBMT, Pôle de Protection des Plantes, 7 chemin de l'IRAT, Saint-Pierre, Ile de la Réunion, 97410, France.
Alexandre
A
De Bruyn
CIRAD, UMR PVBMT, Pôle de Protection des Plantes, 7 chemin de l'IRAT, Saint-Pierre, Ile de la Réunion, 97410, France.|Université de la Réunion, UMR PVBMT, Pôle de Protection des Plantes, 7 chemin de l'IRAT, Saint-Pierre, Ile de la Réunion, 97410, France.|FOFIFA, Laboratoire de Pathologie Végétale, BP 1444, Ambatobe, Madagascar.
Mireille
M
Harimalala
CIRAD, UMR PVBMT, Pôle de Protection des Plantes, 7 chemin de l'IRAT, Saint-Pierre, Ile de la Réunion, 97410, France.|LSBAD, Université de Bangui, BP908, Bangui, Centrafrique, France.
Innocent
I
Zinga
South African National Bioinformatics Institute, Medical Research Council Bioinformatics Unit, University of the Western Cape, Cape Town, South Africa.
Batsirai M
BM
Mabvakure
CIRAD, UMR PVBMT, Pôle de Protection des Plantes, 7 chemin de l'IRAT, Saint-Pierre, Ile de la Réunion, 97410, France.
Murielle
M
Hoareau
CIRAD, UMR PVBMT, Pôle de Protection des Plantes, 7 chemin de l'IRAT, Saint-Pierre, Ile de la Réunion, 97410, France.|CIRAD, UMR BGPI, Campus International de Baillarguet, Montpellier, 34398, France.
Virginie
V
Ravigné
School of Biological Sciences and Biomolecular Interaction Centre, University of Canterbury, Private Bag 4800, Christchurch, New Zealand.
Matthew
M
Walters
CIRAD, UMR PVBMT, Pôle de Protection des Plantes, 7 chemin de l'IRAT, Saint-Pierre, Ile de la Réunion, 97410, France.|Université de la Réunion, UMR PVBMT, Pôle de Protection des Plantes, 7 chemin de l'IRAT, Saint-Pierre, Ile de la Réunion, 97410, France.
Bernard
B
Reynaud
School of Biological Sciences and Biomolecular Interaction Centre, University of Canterbury, Private Bag 4800, Christchurch, New Zealand.|Department of Plant Pathology and Emerging Pathogens Institute, University of Florida, Gainesville, FL, 32611, USA.|Structural Biology Research Unit, University of Cape Town, Rondebosch, 7701, Cape Town, South Africa.
Arvind
A
Varsani
South African National Bioinformatics Institute, Medical Research Council Bioinformatics Unit, University of the Western Cape, Cape Town, South Africa.
Gordon W
GW
Harkins
Institute of Infectious Disease and Molecular Medicine, University of Cape Town, Observatory 7925, Cape Town, South Africa.
Darren P
DP
Martin
CIRAD, UMR PVBMT, Pôle de Protection des Plantes, 7 chemin de l'IRAT, Saint-Pierre, Ile de la Réunion, 97410, France.
Jean-Michel
JM
Lett
CIRAD, UMR PVBMT, Pôle de Protection des Plantes, 7 chemin de l'IRAT, Saint-Pierre, Ile de la Réunion, 97410, France. pierre.lefeuvre@cirad.fr.
Pierre
P
Lefeuvre
D001499:Bayes Theorem; D053839:Begomovirus / Q000235:genetics*; D005075:Biological Evolution; D004279:DNA, Viral / Q000235:genetics; D014644:Genetic Variation; D008270:Madagascar; D002365:Manihot / Q000821:virology*; D058974:Phylogeography; D010935:Plant Diseases / Q000821:virology; D011995:Recombination, Genetic
D004279:DNA, Viral
Begomoviruses; Cassava; Epidemiology; Madagascar; Phylogeography; Recombination