Wild Wild Triatoma infestansTriatoma infestans, a potential , a potential threat that needs to be monitored threat that needs to be monitored

François NoireauFrançois Noireau

UR 016, IRD, Montpellier, FranceUR 016, IRD, Montpellier, FranceIIBISMED, Facultad de Medicina, UMSS, Cochabamba, BoliviaIIBISMED, Facultad de Medicina, UMSS, Cochabamba, Bolivia

Triatoma infestansTriatoma infestans still remains the most important vector of Chagas still remains the most important vector of Chagas disease in the Southern Cone countriesdisease in the Southern Cone countries

The expected success of large-scale control campaigns relied on its The expected success of large-scale control campaigns relied on its almost exclusively domestic nature, almost exclusively domestic nature, precluding the recolonization of treated areas by insects from sylvatic environment

Current evidence that wild populations are much more widespread Current evidence that wild populations are much more widespread than previously thoughtthan previously thought

Known distributional range of wild Known distributional range of wild Triatoma infestans Triatoma infestans in Boliviain Bolivia

Highland foci Highland foci

Inter-Andean Dry ForestInter-Andean Dry Forest 1,600 - 2,800 m asl1,600 - 2,800 m asl

Lowland fociLowland fociGran ChacoGran Chaco< 500 m asl< 500 m asl

Existence of wild Existence of wild T. infestansT. infestans in periurban environments in periurban environments

Cochabamba Cochabamba (> 500,000 inhabitants):(> 500,000 inhabitants):

soaring urbanization near soaring urbanization near wild vectors refugeswild vectors refuges

Chromatic plasticity displayed by wild Chromatic plasticity displayed by wild T. infestansT. infestans

Common morphCommon morph ““Mataral” morphMataral” morphDark morphDark morph

The different morphs of wild The different morphs of wild T. infestansT. infestans

Name Common morph "Mataral" morph Dark morph

Distinguishing morphochromatic traits

- Large size

Markings on the connexivum

Overall dark coloration Markings on the

connexivum

Area of endemism Inter-Andean D ry

Forest (>2,000 m asl)

Inter-Andean D ry Forest, SE Cochaba mba

(~1,700 m asl)

Gran Chaco (<500 m asl)

Habitat Rupicolous Rupicolous Arboreal

Host-feeding Small mammals Small mammals Probably birds

T. cruzi infection rates High High Low

Natural ecotopesNatural ecotopes of Andean wild of Andean wild T. infestansT. infestans

Fallen rocks

Rocky outcropsRocky outcrops

CliffsCliffs

Bioecological traits of a wild Andean Bioecological traits of a wild Andean T. infestans T. infestans populationpopulation

• 30% of the rocky refuges contained 30% of the rocky refuges contained

T. infestansT. infestans

• > 90% of nymphal instars> 90% of nymphal instars

• One generation of triatomines per year One generation of triatomines per year

• Hosts and Hosts and T. cruziT. cruzi reservoirs: rodents reservoirs: rodents

and marsupials and marsupials

• T. cruziT. cruzi infection in vectors > 60% (TcI) infection in vectors > 60% (TcI)

Cochabamba valley, 2,700 m asl, rocky outcroCochabamba valley, 2,700 m asl, rocky outcropsps

Bioecological traits of the Chacoan Bioecological traits of the Chacoan “dark morph” “dark morph” T. infestansT. infestans

• Natural ecotopes of Natural ecotopes of T. infestansT. infestans “dark “dark

morph”: hollow trees, cotorra nests morph”: hollow trees, cotorra nests

((Myiopsitta monachus ) and bromelias ) and bromelias

• 10% of the emergent trees contained 10% of the emergent trees contained

T. infestansT. infestans

• > 90% of nymphal instars> 90% of nymphal instars

• Host: parrot (Amazona aestiva)*

• T. cruziT. cruzi infection in vectors < 3% infection in vectors < 3%

Tita, 350 m aslTita, 350 m asl

* Ceballos * Ceballos et alet al. 2009. 2009

The origin of The origin of T. infestansT. infestans as a species as a species

• First hypothesis: Chacoan origin of First hypothesis: Chacoan origin of T. infestansT. infestans: : based on the based on the occurrence, in the Chaco, of the occurrence, in the Chaco, of the other species with which other species with which T. infestansT. infestans is closely relatedis closely related

• Second hypothesis: Andean origin of Second hypothesis: Andean origin of T. infestansT. infestans: : allozymes, genome size allozymes, genome size and nuclear rDNA favor this and nuclear rDNA favor this hypothesishypothesis

The origin of T. infestans domestic populations

Traditional speculationTraditional speculation

Step 1: domestication of wild guinea pigs by Andean tribes about 5,000 BC

Step 2: dispersal of domestic vectors in association with human migrations

The origin of T. infestans domestic populations

New speculationNew speculation

Step 1: transport and distribution Step 1: transport and distribution of maize hosting the associated of maize hosting the associated fauna (wild rodents and insects) fauna (wild rodents and insects) through the Inca Empirethrough the Inca Empire

Step 2: dispersal of domestic Step 2: dispersal of domestic vectors in association with human vectors in association with human migrationsmigrations

During the Inca period, maize During the Inca period, maize production and storage in the production and storage in the Cochabamba valleyCochabamba valley

Key question: threat represented by wild Key question: threat represented by wild

populations of populations of T. infestansT. infestans

Can wild populations of T. infestans recolonize insecticide-Can wild populations of T. infestans recolonize insecticide-

treated villages and thus jeopardize control efforts?treated villages and thus jeopardize control efforts?

Several observations support the epidemiological Several observations support the epidemiological

risk represented by the wild risk represented by the wild T. infestansT. infestans

1. Maximum distribution reached during the 1970’s 1. Maximum distribution reached during the 1970’s (Gorla 2002)(Gorla 2002)

1 2

2. Current distribution 2. Current distribution (Schofield et al. 2006)(Schofield et al. 2006)

Records of wild Records of wild T. infestansT. infestans

Domestic Domestic T. infestansT. infestans persist in areas where occur wild vectors persist in areas where occur wild vectors

1. Concerning the apparent distribution of 1. Concerning the apparent distribution of T. infestansT. infestans

Various haplotypes (COI and Cytb genes) are shared by Various haplotypes (COI and Cytb genes) are shared by both domestic and sylvatic Andean populationsboth domestic and sylvatic Andean populations

The distinct "Mataral form”, found in sylvatic The distinct "Mataral form”, found in sylvatic environment in the southeastern Cochabamba environment in the southeastern Cochabamba department, is also colonizing houses of the department, is also colonizing houses of the same regionsame region

2. Concerning the genetic and morphochromatic 2. Concerning the genetic and morphochromatic variability observed in variability observed in T. infestansT. infestans

3. Concerning the process of domestication of 3. Concerning the process of domestication of T. infestansT. infestans

T. infestansT. infestans was, without any doubt, the triatomine was, without any doubt, the triatomine species that displayed the most successfully completed species that displayed the most successfully completed process of domestication process of domestication

It is difficult to give credit to the hypothesis that wild forms It is difficult to give credit to the hypothesis that wild forms of of T. infestansT. infestans would since then have become restricted to would since then have become restricted to their natural habitattheir natural habitat

Genetic diversity and dispersal ability in wild Genetic diversity and dispersal ability in wild T. infestansT. infestans at high altitude:at high altitude: collecting sites collecting sites

Rocky outcropsRocky outcrops

Large block of rocksLarge block of rocks

HousesHouses

Northern hillNorthern hillWestern hillWestern hill

Southern hillSouthern hill

Cochabamba valley, 2,700 m aslCochabamba valley, 2,700 m asl

Genetic diversity of wild Genetic diversity of wild T. infestansT. infestans based on based on

the mitochondrial CytB genethe mitochondrial CytB gene

T. infestansT. infestans collected in the sylvatic collected in the sylvatic sites (3  hills and large outcrops) sites (3  hills and large outcrops) display genetic variation (7 hapl.)display genetic variation (7 hapl.)

C

Western hillWestern hill

Northern hillNorthern hill

Southern hillSouthern hill

Large outcropsLarge outcrops

HousesHouses T. infestansT. infestans from the houses from the houses

display only one haplotype (C) display only one haplotype (C) also detected in wild triatominesalso detected in wild triatomines

Two sylvatic haplotypes (A & C) Two sylvatic haplotypes (A & C) were found in domestic bugs from were found in domestic bugs from the region of Sucre*the region of Sucre*

Domestic triatomines from Cochabamba and Sucre Domestic triatomines from Cochabamba and Sucre display haplotypes also detected in sylvatic bugsdisplay haplotypes also detected in sylvatic bugs

* Giordano * Giordano et alet al. 2005. 2005

46 46 T. infestans T. infestans characterizedcharacterized

Dispersal abilityDispersal ability

T. infestansT. infestans does not disperse by flying at high altitude does not disperse by flying at high altitude

MMicrosatellite loci used to detect gene flow between neighboring collecting sites icrosatellite loci used to detect gene flow between neighboring collecting sites (< 1 km(< 1 km22))

T. infestansT. infestans disperses over disperses over continuous land cover (high continuous land cover (high significant significant FstFst values) values)

T. infestansT. infestans does not disperse does not disperse over land cover disrupted by over land cover disrupted by man made activitiesman made activities

Northern hillNorthern hillWestern Western hillhill

SouthernSouthernhillhill

Large PD rocksLarge PD rocks

Current hypothesesCurrent hypotheses

Evidences do not support a Evidences do not support a continued flowcontinued flow of of T. infestansT. infestans between sylvatic refuges and domestic environmentsbetween sylvatic refuges and domestic environments

In the Andes, the crepuscular coldness restricts flight dispersal and may In the Andes, the crepuscular coldness restricts flight dispersal and may hamper the process of domestic intrusion by wild hamper the process of domestic intrusion by wild T. infestansT. infestans

In the Chaco, the emergent trees are become scarce in the vicinity of the In the Chaco, the emergent trees are become scarce in the vicinity of the villages. Consequently, the villages. Consequently, the T. infestansT. infestans "dark morph" would persist in "dark morph" would persist in preserved and remote wooded areaspreserved and remote wooded areas

Finally, only unusual circumstances would generate a transfer Finally, only unusual circumstances would generate a transfer of of T. infestansT. infestans from the natural to the domestic environment from the natural to the domestic environment

ObrigadoObrigado

IIBISMED Cochabamba: IIBISMED Cochabamba: Team of Lineth GarciaTeam of Lineth Garcia

PNCH: PNCH: Mirko RojasMirko Rojas

FAN Santa Cruz: FAN Santa Cruz: Teresa GutierrezTeresa Gutierrez

IRD Montpellier: IRD Montpellier: Team of Pierre KengneTeam of Pierre Kengne

ETS Cochabamba: ETS Cochabamba: Roberto RodriguezRoberto Rodriguez

Agradecimientos:Agradecimientos:

IOC FIOCRUZ Rio de Janeiro: IOC FIOCRUZ Rio de Janeiro: Teams of José Jurberg and Ana Maria JansenTeams of José Jurberg and Ana Maria Jansen