Is Culicoides imicola (Diptera: Ceratopogonidae) a recent invasive species in the Mediterranean basin?

(1)

Is

Culicoides

imicola

(Diptera:

Ceratopogonidae) a recent invasive

species in the Mediterranean basin?

Funded by

Cirad and CHERCHAV Convention

Stéphanie Jacquet, Karine Huber, Jérémy Bouyer, Christine Chevillon, Thomas Balenghien, Claire Garros

(2)

Biological invasions

Their consequences

 Ecosystem modification and/or deterioration

 Detrimental effects on agriculture

 Impacts on health

The causes

 Phenotypic traits, evolutionary change

 Migration

(3)

An example:

Culicoides imicola

and

(4)

C. imicola

, a vector species

Arthropoda: Diptera: Ceratopogonidae

 Small biting midge with passive dispersal through winds

 Vector of economically important viruses of livestock :

- African horse sickness virus (AHSV) - Bluetongue virus (BTV)

- Epizootic hemorrhagic disease virus (EHDV)

(5)

C. imicola

, a vector species

Arthropoda: Diptera: Ceratopogonidae

 Small biting midge with passive dispersal through winds

 Vector of economically important viruses of livestock :

- African horse sickness virus (AHSV) - Bluetongue virus (BTV)

- Epizootic hemorrhagic disease virus (EHDV)

(6)

C. imicola

and BTV distribution

before 1998

?

1998

 C. imicola limited to North Africa and Arabic peninsula  BTV distributed in America, Asia, Australia and Africa

(7)

?

1998

 In 1998, BT outbreaks in southern Europe

Date of last outbreak Serotype

Altitude 0 - 100 100 - 250 250 - 500 1000 - 2000 2000 – 3000 3000 - 4000 2004-06 4 2003 4 2000 2 2003-04 2000-02 2 1999- 2002 2 2000-06 2000-06 2001 6 4 16 2 4 9 16 2 4 16 _{2001 1} 2001 1 2002 9 2004 9 2003 16 4 9 2004 16 1999 9 2000916 500 - 1000 2004-06 4 1999 4 2006 1 2004-06 4 2006 1 2006 1 1999 16 2004-06 4 2003 4 2000 2 2003-04 2000-02 2 1999- 2002 2 2000-06 2000-06 2001 6 4 16 2 4 9 16 2 4 16 _{2001 1} 2001 1 2002 9 2004 9 2003 16 4 9 2004 16 1999 9 2000916 500 - 1000 2004-06 4 1999 4 2006 1 2004-06 4 2006 1 2006 1 1999 16 BTV-1 BTV-6 BTV-1 BTV-6 BTV-2 BTV-16 BTV-9 BTV-4 BTV-2 BTV-16 BTV-2 BTV-2 BTV-16 BTV-16 BTV-9 BTV-4 BTV-4 BTV-4 2006 1 BTV-1 BTV-1

C. imicola

and BTV distribution

(8)

?

1998

2005

Date of last outbreak Serotype

Altitude 0 - 100 100 - 250 250 - 500 1000 - 2000 2000 – 3000 3000 - 4000 2004-06 4 2003 4 2000 2 2003-04 2000-02 2 1999- 2002 2 2000-06 2000-06 2001 6 4 16 2 4 9 16 2 4 16 _{2001 1} 2001 1 2002 9 2004 9 2003 16 4 9 2004 16 1999 9 2000916 500 - 1000 2004-06 4 1999 4 2006 1 2004-06 4 2006 1 2006 1 1999 16 2004-06 4 2003 4 2000 2 2003-04 2000-02 2 1999- 2002 2 2000-06 2000-06 2001 6 4 16 2 4 9 16 2 4 16 _{2001 1} 2001 1 2002 9 2004 9 2003 16 4 9 2004 16 1999 9 2000916 500 - 1000 2004-06 4 1999 4 2006 1 2004-06 4 2006 1 2006 1 1999 16 BTV-1 BTV-6 BTV-1 BTV-6 BTV-2 BTV-16 BTV-9 BTV-4 BTV-2 BTV-16 BTV-2 BTV-2 BTV-16 BTV-16 BTV-9 BTV-4 BTV-4 BTV-4 2006 1 BTV-1 BTV-1

 In 1998, BT outbreaks in southern Europe

 C. imicola found in new areas

C. imicola

and BTV distribution

(9)

Purse et al.. 2007, Purse et al.,2005

An hypothesis: climate change

 Increase temperature have lead to

C. imicola

range

expansion

Predicted probability of the presence of Culicoides imicola s.s

0 0-1 0-2 0-3 0-4 0-5 0-6 0-7 0-8 0-9 No

prediction

(10)

Recent or ancient colonization ?

knowledge from genetic data

Nolan et al, 2008

Phylogeographic studies based on COI

 Recent colonization

 Two routes of colonization

Maldyun et al, 2013

Population genetics study based on microsatellites

 Observed diversity and structure

(11)

Recent colonization

vs

entomological

surveys bias ?

Venail et al.. 2012. Conte et al.. 2009

 Population expansion in Var department (France)

Date of last outbreak Serotype Altitude 0 - 100 100 - 250 250 - 500 1000 - 2000 2000 – 3000 3000 - 4000 2004-06 4 2003 4 2000 2 2003-04 2000-02 2 1999- 2002 2 2000-06 2000-06 2001 6 4 16 2 4 9 16 2 4 16 2001 1 2001 1 2002 9 2004 9 2003 16 4 9 2004 16 1999 9 2000 916 500 - 1000 2004-06 4 1999 4 2006 1 2004-06 4 2006 1 2006 1 1999 16 2004-06 4 2003 4 2000 2 2003-04 2000-02 2 1999- 2002 2 2000-06 2000-06 2001 6 4 16 2 4 9 16 2 4 16 2001 1 2001 1 2002 9 2004 9 2003 16 4 9 2004 16 1999 9 2000 916 500 - 1000 2004-06 4 1999 4 2006 1 2004-06 4 2006 1 2006 1 1999 16 BTV-1 BTV-6 BTV-1 BTV-6 BTV-2 BTV-16 BTV-9 BTV-4 BTV-2 BTV-16 BTV-2 BTV-2 BTV-16 BTV-16 BTV-9 BTV-4 BTV-4 BTV-4 2006 1 BTV-1 BTV-1

(12)

Hypothesis (1):

One source = Sub-Saharan Africa

 Determine if

C. imicola

is a recent invader

- Spatial scenarios : origin ?

- Temporal scenarios : recent vs ancient ?

Hypothesis (2):

Two sources = Sub-Saharan Africa and Middle-East

Aims and scenarios

Sub-Saharan Africa North Africa Middle East West Mediterranean basin East Mediterranean basin Sub-Saharan Africa North Africa Middle East West Mediterranean basin East Mediterranean basin

(13)

Material

 55 populations

West Mediterranean basin (WMB) East Mediterranean basin (EMB)

West Africa (WA)

South-East Africa (SEA)

 2 mitochondrial and 1

nuclear genes

8 individuals/site

Cytochrome Oxidase subunit I (COI, 476bp) , Cytochrome B (CytB, 635bp), Elongation factor

alpha (Efα, 556bp)  9 microsatellites markers 32 individuals/site Mali Burkina Faso Cameroon Ethiopia Madagascar France Algeria Benin Itaiy Spain Portugal Morocco Senegal South Africa Reunion Mauritius Mozambique Kenya Greece Tunisia Israel Zimbabwe Turkey UAE

(14)

Methods

 Diversity index

 Genealogy relationships: haplotype network, phylogeny

 Demographic features: neutrality and mismatch test

 Populations structure: bayesian clustering analysis,

(15)

Results : Population genetic relationships

N J network COI polymorphism South Africa Benin Burkina Faso Cameroon Ethiopia Greece Israel Kenya Madagascar Mali Mauritius Mozambique Reunion Senegal Turkey Zimbabwe Algeria Baleares Corsica Spain Italy France Morocco Portugal Sardinia Sicily Tunisia

 Higher diversity in Sub-Saharan Africa =>

(16)

Results : Population genetic relationships

N J network COI polymorphism South Africa Benin Burkina Faso Cameroon Ethiopia Greece Israel Kenya Madagascar Mali Mauritius Mozambique Reunion Senegal Turkey Zimbabwe Algeria Baleares Corsica Spain Italy France Morocco Portugal Sardinia Sicily Tunisia

historical range

(17)

Results : Population genetic relationships

N J network COI polymorphism

WMB South Africa Benin Burkina Faso Cameroon Ethiopia Greece Israel Kenya Madagascar Mali Mauritius Mozambique Reunion Senegal Turkey Zimbabwe Algeria Baleares Corsica Spain Italy France Morocco Portugal Sardinia Sicily Tunisia

historical range

 Two genetic groups

 No shared haloptypes between WMB and

(18)

Results : Population genetic relationships

N J network COI polymorphism

WMB South Africa Benin Burkina Faso Cameroon Ethiopia Greece Israel Kenya Madagascar Mali Mauritius Mozambique Reunion Senegal Turkey Zimbabwe Algeria Baleares Corsica Spain Italy France Morocco Portugal Sardinia Sicily Tunisia

historical range

 Two genetic groups

 No shared haloptypes between WMB and

EMB

 Star-like network in the

WMB => recent demographic expansion?

(19)

West Mediterranean basin East Mediterranean basin West Africa South-East Africa H a p _ 1 1 6 H a p _ 8 3 H a p _ 6 2 Hap _ 9 4 H a p _ 1 8 Hap_11 H a p _ 1 0 Hap _ 6 8 Hap_59 H a p _ 5 0 H a p _ 5 5 H a p _ 8 2 H a p _ 1 1 0 H a p _ 1 1 5 Hap_88 H a p _ 2 0 H a p _ 1 6 Hap_76 Hap_10 1 H a p _ 7 0 H a p _4 7 H a p _ 3 4 Hap _ 1 0 6 H a p _ 3 8 H a p _ 1 2 Hap _ 1 7 H a p _ 5 1 H a p _ 8 1 H a p _ 2 5 Hap_14 H ap _ 64 H a p _ 7 3 H a p _ 9 8 H a p _ 9 3 H a p _ 1 1 7 Hap _ 2 3 Hap_7 Hap _ 7 8 H ap _ 48 H a p_ 52 Hap_91 Hap _ 7 7 Hap_10 0 H a p _ 4 9 Hap_6 Hap _ 7 1 Hap_42 H a p _ 8 0 H a p _ 2 4 H a p _ 4 6 H a p _ 8 H a p _ 4 1 H a p _ 2 9 H a p _ 6 7 H a p _ 1 3 H a p _ 3 7 H a p _ 6 5 H a p _ 9 5 H a p _ 5 7 H a p _ 3 9 H a p _ 1 0 8 H a p _ 4 H a p _ 9 2 H a p _ 8 6 H a p _ 1 0 4 H a p _ 3 5 H a p _ 3 3 H a p _ 9 7 H a p _ 4 4 H a p _ 4 5 H a p _ 1 H a p _ 2 6 H a p _ 1 1 3 H a p _ 3 1 H a p _ 3 H a p _ 3 0 H a p _ 2 H a p _ 1 0 5 H a p _ 1 1 1 H a p _ 2 2 H a p _ 7 9 H a p _ 9 6 H a p _ 8 5 H a p _ 7 4 H a p _ 1 1 2 H a p _ 1 0 3 H a p _ 5 6 H a p _ 3 6 H a p _ 6 9 H a p _ 1 0 7 H a p _ 5 3 H a p _ 8 9 H a p _ 5 H a p _ 9 0 H a p _ 1 9 H a p _ 7 5 H a p _ 2 1 H a p _ 4 0 H a p _ 8 7 H a p _ 6 6 H a p _ 6 1 H a p _ 6 0 H a p _ 3 2 H a p _ 9 9 H a p _ 9 H a p _ 5 8 H a p _ 8 4 H a p _ 6 3 H a p _ 1 1 4 H a p _ 1 0 9 H a p _ 1 5 H a p _ 2 8 H a p _ 2 7 H a p _ 7 2 H a p _ 5 4 H a p _ 4 3 H a p _ 1 0 2 1 0 ,7 8 0 ,9 8 0 ,9 7 1 0 ,6 1 0 ,9 9 0 ,8 1 0 ,7 3 1 0 ,9 5 4 7 0 ,9 8 0 ,7 9 0 ,7 5 0 ,7 8 0,7 0 0 ,9 8 0 ,9 9 0 ,9 5 0 ,7 1 0 ,9 8 0 ,6 8 0 ,8 5 0 ,9 0 5 2 0 ,6 4 3 2 0 ,7 0 0 ,9 4 0 ,8 3 0,9 9 0 ,8 5 0 ,5 6 0 ,9 7 0 ,9 9 BA tree, COI+Cytb  WMB genetically closer to WA

 EMB genetically related to WA and SEA

(20)

ZW DZ2 ES01 SN10 DZ7 ET IL01 PO10 Es04 FrV0 SN19 BJ MA3 SN08 SN04 PO5 ItTo SN21 ItSs Es03 ZA1 FrV33 DZ4 MA1 Cb6 Cb5 Re FrV1 SN13 Es02 Cb4 ItCa PT09 IL06 Es06 DZ10 Ca5 ItSi MZ PO3 PT05 FrA IL04 CM Grece PT03 Ca1 SN09 ZA2

 Genetic differentiation in Sub-Saharan Africa

NJ based on microsatellite polymorphism

West Mediterranean basin East Mediterranean basin West Africa

South-East Africa

(21)

North Africa Southern Europe WA SEA Southern Europe 0.051* - WA 0.520** 0.603** - SEA 0.614** 0.700** 0.236** - EMB 0.635** 0.715** 0.358** 0.167**

 Low genetic differentiation

between Mediterranean basin populations Mali Burkina Faso Cameroon Ethiopia Madagascar France Algeria Benin Italiy Spain Portugal Morocco Senegal South Africa Reunion Mauritius Mozambique Kenya Greece Tunisia Israel Zimbabwe

Clusters based on COI polymorphism Turkey

(22)

North Africa Southern Europe WA SEA Southern Europe 0.051* - WA 0.520** 0.603** - SEA 0.614** 0.700** 0.236** - EMB 0.635** 0.715** 0.358** 0.167**

 Low genetic differentiation

between Mediterranean basin populations

 High genetic diffentiation

between WMB and EMB +

African populations Mali Burkina Faso Cameroon Ethiopia Madagascar France Algeria Benin Italiy Spain Portugal Morocco Senegal South Africa Reunion Mauritius Mozambique Kenya Greece Tunisia Israel Zimbabwe

Clusters based on COI polymorphism Turkey

(23)

Clusters based on microsatellite polymorphism Mali Burkina Faso Cameroon Ethiopia Madagascar France Algeria Benin Italiy Spain Portugal Morocco Senegal South Africa Reunion Mauritius Mozambique Kenya Greece Tunisia Israel Zimbabwe WMB Central

MB Greece Israel SEA Central MB 0.016** - Greece 0.147** 0.113** - Israel 0.148** 0.114** 0.078** - SEA 0.097** 0.077** 0.137** 0.092** - Senegal 0.104** 0.078** 0.131** 0.128** 0.034**

 High genetic differentiation

between WMB and EMB

(24)

Clusters based on microsatellite polymorphism Mali Burkina Faso Cameroon Ethiopia Madagascar France Algeria Benin Italiy Spain Portugal Morocco Senegal South Africa Reunion Mauritius Mozambique Kenya Greece Tunisia Israel Zimbabwe WMB Central

MB Greece Israel SEA Central MB 0.016** - Greece 0.147** 0.113** - Israel 0.148** 0.114** 0.078** - SEA 0.097** 0.077** 0.137** 0.092** - Senegal 0.104** 0.078** 0.131** 0.128** 0.034**

 High genetic differentiation

between WMB and EMB

 High diffentiation between

WMB, EMB and sub-Saharan

Africa

(25)

Results: Populations demographic history

W MB WA EMB SEA WMB WA EMB SEA WMB WA  Significant deviation from neutrality

(COI+Cytb, Efα) for

WA and WMB

 Demographic stability

for SEA and EMB,

while signature of

population expansion

(26)

Sub-Saharan Africa = historical range Recent demographic expansion of West Mediterranean basin populations only

Conclusion

Population diversity and demography

 High diversity in Sub-saharan Africa but low diversity in

the Mediterranean basin

 Star like shape network + significant neutrality and

(27)

Population origin and structure

 No shared haplotypes between Sub-saharan Africa and West Mediterranean basin but West Mediterranean basin

genetically closer to West Africa

 No shared haplotypes + high genetic differentiation between West and East Mediterranean basin

 East Mediterranean basin genetically closer to South-East Africa

Long time presence of

C. imicola

in EMD

Genetic subdivision between WMD and EMD

Conclusion

(28)

Support one source hypothesis with two routes of colonization : Atlantic coast and Nile valley

Sub-Saharan Africa North Africa Middle East West Mediterranean basin East Mediterranean basin T ≈ 0 _{T >> 0}

=> supported by ABC analyses P=0,56

Conclusion

(29)

Acknowledgements

Mali Burkina Faso Cameroon Ethiopia Madagascar France Algeria Benin Italiy Spain Portugal Morocco Senegal South Africa Reunion Mauritius Mozambique Kenya Greece Tunisia Israel Zimbabwe A Chaskopoulou USDA, Greece Y Gottlieb HUJ, Israel M Kasina KARI, Kenya G Venter K Labuschagne OVI, South Africa J Lucientes UZ, Spain M Miranda UIB, Spain N Pagès CReSA, Spain D Ramilo, I Fonseca CIISA, Portugal A Tabbabi Tunisia A Gueye Fall M Fall M Tallar Seck ISRA, Senegal M Goffredo IZS, Italy

(30)

Acknowledgements

Mali Burkina Faso Cameroon Ethiopia Madagascar France Algeria Benin Italiy Spain Portugal Morocco Senegal South Africa Reunion Mauritius Mozambique Kenya Greece Tunisia Israel Zimbabwe A Chaskopoulou USDA, Greece Y Gottlieb HUJ, Israel M Kasina KARI, Kenya G Venter K Labuschagne OVI, South Africa J Lucientes UZ, Spain M Miranda UIB, Spain N Pagès CReSA, Spain D Ramilo, I Fonseca CIISA, Portugal A Tabbabi Tunisia A Gueye Fall M Fall M Tallar Seck ISRA, Senegal M Goffredo IZS, Italy

M-L Setier-Rio (EID-Méd, France) M de Garine-Wichatitsky, T Martin,

C Cêtre-Sossah, T Baldet, A Desvars, F Starchurski (Cirad,

France)

B Mathieu, J-C Delécolle (UdS, France)

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