Abstract
BackgroundCassava 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.ResultsThe 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.ConclusionsOur 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0749-2) contains supplementary material, which is available to authorized users.
Highlights
Introduction eventsIntroduction dates (95 % highest posterior density (HPD)) 1996–2004 [1995–2005] [1924–1986]1988–1990 [1982–1997] 1988–1996 [1983–2003] [1921–1989]1984–2003 [1971–2006][2.82 × 10−3; 4.89 × 10−3] [4.13 × 10−4; 7.14 × 10−4]1997–1999 [1994–2003] 1.69 × 10−3 [1.31 × 10−3 to 2.12 × 10−3][9.57 × 10−4; 1.28 × 10−3]For each dataset, the total and Madagascan (MG) number of sequences, mean and range of identity percentages are indicated ([FS] = Full Sequence, [core CP] = core of the capsid protein encoding ORF), as well as the number of recombinant Madagascan sequences isolated in this study
The occurrence of six cassava mosaic geminivirus (CMG) species in Madagascar Besides PCR typing data on a large number of infected Madagascan cassava samples [22], prior to this study very little sequence information was available for CMGs circulating on the island
As part of this study, a total of 279 full DNA-A and 117 full DNA-B components were cloned and sequenced from 173 symptomatic Madagascan cassava leaves sampled during an epidemiological survey conducted between 2009 and 2011 [22] as well as 91 additional samples collected on the island between 2005 and 2008
Summary
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. It is possible that the instability of some of these “unnatural” interactions, has in many cases triggered the emergence of devastating new viral diseases [2] In this regard, the cultivation of cassava in Africa represents an excellent example both of how the introduction of exotic plant species into foreign ecosystems can provide opportunities for novel interactions, and of how such interactions can have far-reaching socio-economic consequences. Caused by a diverse group of at least nine distinct native African virus species that are collectively referred to as cassava mosaic geminiviruses (CMGs, genus: Begomovirus; family: Geminiviridae), CMD has evolved to become one of the most socio-economically damaging crop pathogens to have ever existed
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