Dispersal processes underlying the recent pandemic caused by the plant pathogenic fungus

0 0.05 0.1 0.15 0.2 0.25 0.3 0.35 0 1 2 3 4 5 6 10 Km

Populations of ~ 30 ind. in the same locality Sparsed individuals

Sampling of individuals and populations among a global collection of isolates

Australia N. Caledonia Fidji Malaysia Philippines Vanuatu Tonga Samoa Cook Islands Futuna PNG Indonesia Viet Nam China Panama Costa Rica Jamaica Mexico Ecuador Florida Cuba Honduras Colombia Venezuela Dom. Rep. C.Ivoire Comoros Cameroun Nigeria Uganda Mayotte Gahna Congo Tanzania Rwanda Burundi

AREAS of INTRODUCTION AREA of ORIGIN

1978 Gabon 1973 ? Zambie 1972 Honduras 1963 Fidji

- Infected plant material - Ascospores (sexual cycle) - Conidia (asexual cycle)

- Existence of sexual reproduction - Stable and panmictic populations

- Historical data about global spread available

A convenient biological model for population genetics and phylogeographic studies:

Dispersal modes of M. fijiensis:

Life cycle of Mycosphaerella fijiensis From Agrios, George N. 2005.

COM UGA CAM CAM CIV GAB NGA COL CR HND HND MEX PAN VEN JAM RD

IND MYS PHL PNG FIJ NCL AUS Fst = 0.57 Fst = 0.40 Fst = 0.20 He = 0.35 He = 0.22 _{He = 0.65} He = 0.32 Fst = 0.21

S. ROBERT*, A. RIEUX*, F. HALKETT†, M-F. ZAPATER*, L. DE LAPEYRE DE BELLAIRE‡, C. ABADIE*, V. RAVIGNE* and J. CARLIER*



Explorative population genetics analysis



Molecular phylogenetic analysis

23 populations (~700 individuals) 21 microsatellite markers

(Zapater

et al

, 2008 Mol. Ecol. Res.; Robert

et al

, 2010 Am. J. Bot.)

120

M. fijiensis

individuals

8 sequence-based nuclear markers

Phylogenetic tree reconstructed by the maximum likelihood method

How plant pathogenic fungi spread is the first question to consider for understanding the emergence of diseases caused by such organisms.

The ascomycete fungus

Mycosphaerella fijiensis,

causing the black leaf streak disease of banana, is an example

of a recent pandemic in agriculture and a good model to address this question in the case of an aerial plant

pathogen. The pandemic started around 1960 from the South-East Asia and

M. fijiensis

has spread to almost all

banana producing areas for the last 40 years.



Perspective: test different scenarii and estimate parameters using ABC (Approximate Bayesian Computation) method



CONTEXT & OBJECTIVES



PHYLOGEOGRAPHY STUDY AT GLOBAL SCALE



SPATIAL GENETIC ANALYSIS AT LOCAL SCALE

Dispersal processes underlying the recent pandemic caused by the plant

pathogenic fungus

Mycosphaerella fijiensis

Previous studies of genetic structure of populations have highlighted a higher genetic diversity in South-East Asia, and high levels of genetic differentiation between and within continents, suggesting

that founder events have accompanied the pandemic (Carlier

et al

, 1996; Rivas

et al

, 2004 Mol. Ecol.).

A further investigation of the dispersal processes underlying the pandemic is now required.

- A pattern of genetic admixture in AMERICA, possibly due to multiple introductions - An only successful introduction in AFRICA, probably associated with a bottleneck, explaining emergence of an homogeneous group comparatively to the other continents

These different analysis were congruent and suggested strong hypotheses:

- Asian origins for all these introduction events certainly from transport of infected plant materials

Low level of intraspecific polymorphism

Markers of old events of introductions High level of polymorphism Markers of fine-scale dispersal processes

Objectives:

 To infer historical and demographic events (bottlenecks, admixture) undergone by invading populations

 To reconstruct global routes of dissemination and clarify dispersal modes of the pathogen

Diversity and differentiation indices, Clustering analysis (STRUCTURE)

NJ tree Cavalli-Sforza distances Nigeria Cameroon Gabon 1978 1980 Avr. 1983 1986

Moungo producing area

Disease mentions 0 0,2 0,4 0,6 0,8 1 0.0 0.5 1.0 He = 0.43 Fst= 0.1 FST / (1 -FST ) Log distance (km)

P=0.13 (all the samples) P<0.05 (Samples 1 to 5)

The Cameroon situation,

an example of a recently

(



_{1980) colonized area}

10 Populations (~ 290 individuals) 19 microsatellite markers

Diversity and differentiation indices, Clustering analysis (STRUCTURE)

Isolation by distance analysis (discrete populations)

F(1-F) = f (Ln(d)) y = 0,004x + 0,0097 -0,4 -0,3 -0,2 -0,1 0 0,1 0,2 0,3 0,4 0,5 -5 -4,5 -4 -3,5 -3 -2,5 -2 -1,5 -1 Ln (d) F/(1-F) Distance géographique Diff ér enc iat ion g én éti que 5 Forest 6

-A genetic discontinuity was detected at the middle of the transect (between sites 5 and 6)

- An Isolation by distance was detected before the above discontinuity suggesting gradual dispersal through ascospores

2D sampling (105 sites, 570 individuals) 17 microsatellite markers

1D sampling on a 30-km-long transect (90 sites, 321 individuals)

17 microsatellite markers

Isolation by distance analysis (continuous populations)

Spatial clustering analysis (GENELAND)

- The genetic discontinuity was sharp delimiting 2 populations. No landscape

features matched this discontinuity  _{colonization trace (e.g. through gene surfing)}

- No isolation by distance  _{high effective population size in}

M.fijiensis

_is

suspected



Perspective: estimate dispersal from allelic clines detected

between the 2 populations

* CIRAD, UMR BGPI, Campus international de Baillarguet, TA A-54K, F-34398 Montpellier Cedex 5, France. Correspondence: jean.carlier@cirad.fr † Present adress; INRA, Nancy-Université, UMR 1136 Interactions Arbre-Microorganismes, F-54280 Champenoux, France.

‡ CIRAD, Persyst, UPR Syst. Banan. Ananas, TA B-26 / PS4, Blvd. de la Lironde, 34398 Montpellier Cedex 5, France.



Along a 300-km-long transect

(Halkett

et al

, 2010 Mol. Ecol.)



On a 50x50 km area

(Rieux

et al

, 2011 Mol. Ecol.)

7 7 5 7 53 6 0 9 4 9 8 7 7 8 2 9 2 Africa America Asia Pacific