Open Access

North American import? Charting the origins of an enigmatic Trypanosoma cruzi domestic genotype

  • Federico A Zumaya-Estrada1,
  • Louisa A Messenger2,
  • Teresa Lopez-Ordonez1,
  • Michael D Lewis2,
  • Carlos A Flores-Lopez3,
  • Alejandro J Martínez-Ibarra4,
  • Pamela M Pennington5,
  • Celia Cordon-Rosales5,
  • Hernan V Carrasco6,
  • Maikel Segovia6,
  • Michael A Miles2 and
  • Martin S Llewellyn2Email author
Parasites & Vectors20125:226

https://doi.org/10.1186/1756-3305-5-226

Received: 11 August 2012

Accepted: 3 October 2012

Published: 10 October 2012

Abstract

Background

Trypanosoma cruzi, the agent of Chagas disease, is currently recognized as a complex of six lineages or Discrete Typing Units (DTU): TcI-TcVI. Recent studies have identified a divergent group within TcI - TcIDOM. TcIDOM. is associated with a significant proportion of human TcI infections in South America, largely absent from local wild mammals and vectors, yet closely related to sylvatic strains in North/Central America. Our aim was to examine hypotheses describing the origin of the TcIDOM genotype. We propose two possible scenarios: an emergence of TcIDOM in northern South America as a sister group of North American strain progenitors and dispersal among domestic transmission cycles, or an origin in North America, prior to dispersal back into South American domestic cycles. To provide further insight we undertook high resolution nuclear and mitochondrial genotyping of multiple Central American strains (from areas of México and Guatemala) and included them in an analysis with other published data.

Findings

Mitochondrial sequence and nuclear microsatellite data revealed a cline in genetic diversity across isolates grouped into three populations: South America, North/Central America and TcIDOM. As such, greatest diversity was observed in South America (Ar = 4.851, π = 0.00712) and lowest in TcIDOM (Ar = 1.813, π = 0.00071). Nuclear genetic clustering (genetic distance based) analyses suggest that TcIDOM is nested within the North/Central American clade.

Conclusions

Declining genetic diversity across the populations, and corresponding hierarchical clustering suggest that emergence of this important human genotype most likely occurred in North/Central America before moving southwards. These data are consistent with early patterns of human dispersal into South America.

Keywords

Trypanosoma cruzi Maxicircle Microsatellite Chagas Disease Phylogeography Population genetics TcI

Findings

Trypanosoma cruzi, the aetiological agent of Chagas disease, infects 6-8 million people in Latin America, while some 25 million more are at risk of acquiring the disease[1]. Parasite transmission to mammal hosts, including humans, can occur through contact with the faeces of hematophagous triatomine bugs. However, non-vectorial routes are also recognized, including blood transfusion, organ transplantation, congenital transmission, and oral transmission via ingestion of meals contaminated with infected triatomine feces[2, 3].

T. cruzi (family Trypanosomatidae; Euglenozoa: Kinetoplastida) is most closely related to several widely dispersed species of bat trypanosomes[4]. Salivarian trypanosomes including medically important Trypanosoma brucei subspecies, represent a more divergent group[5]. The age of the split between the T. cruzi-containing and T. brucei-containing trypanosome lineages is thought to have been concurrent with the separation of Africa and South America/Antarctica/Australasia 100MYA[6], implying that T. cruzi and the other Schizotrypanum species evolved exclusively in South America. Others propose an alternative origin of T. cruzi from an ancestral bat trypanosome potentially capable of long range dispersal[7]. Whilst the precise scenario for the arrival of ancestral Schizotrypanum lineages in South America is a matter for debate, the current continental distribution and genetic diversity of T. cruzi supports an origin within South America. Parasite transmission is maintained via hundreds of mammal and triatomine species in different biomes throughout South and Central America, as well as the southern states of the USA[8].

Biochemical and molecular markers support the existence of six lineages or Discrete Typing Units (DTU): TcI, - TcVI agreed by international consensus ([9]. Each DTU can be loosely associated with a particular ecological and/or geographical framework[10]. TcI is ubiquitous among arboreal sylvatic foci throughout the geographic distribution of T. cruzi and is the major agent of human Chagas disease in northern South America. Several molecular tools now identify substantial genetic diversity within TcI[1114]. Importantly these new approaches consistently reveal the presence of a genetically divergent and homogeneous TcI group (henceforth TcIDOM – previously TcIa/VENDOM) associated with human infections from Venezuela to Northern Argentina, and largely absent from wild mammals and vectors sampled to date[14]. The origin of this clade is unclear, although recent work supports a sister group relationship with TcI circulating in North America (e.g.[12, 13]).

In this manuscript we have set out to evaluate the genetic diversity of TcI in North/Central America, undertaking a comparison with TcI diversity in South America, including TcIDOM. Our aim was to examine hypotheses describing the origin of the TcIDOM clade. We propose two possible scenarios: an emergence of TcIDOM in northern South America as a sister group of North American strains and dispersal among domestic transmission cycles, or an origin in North America, prior to dispersal back into South American domestic cycles, possibly anthropically. To provide further insight into this question we undertook high resolution nuclear and mitochondrial genotyping of multiple Central American strains (from areas of México and Guatemala) and included them in an analysis with other published data[1113].

A panel of 72 TcI isolates and clones was assembled for analysis (Table1)[1116]. Of these, existing sequences and microsatellite data were available for 46 isolates[11, 12]. Isolates were classified into three populations: TcINORTH-CENT, TcISOUTH and TcIDOM. TcINORTH-CENT includes samples from the USA, México, Guatemala and Honduras; TcISOUTH corresponds to South America (Argentina, Bolivia, Colombia, Venezuela and Brazil) and TcIDOM with exclusively domestic isolates from Colombia and Venezuela, already known to correspond to a genotype with restricted genetic diversity: TcIa, as previously described by Herrera et al., (2007)[17] and VENDom, as described by Llewellyn et al., (2009)[13]. Additional DTU isolates (TcIII-TcIV) were included as out-groups in the mitochondrial analysis.
Table 1

Trypanosoma cruzi I samples included in this study

Strain code

Strain

Host/vector

Country

State

Latitude

Longitude

Date

Population

Reference

PALDA4

PALDA4

Didelphis albiventris

Argentina

Chaco

-27.133

-61.460

2001

SOUTH

Messenger et al., [12]

PALDA21

PALDA21

Didelphis albiventris

Argentina

Chaco

-27.133

-61.460

2001

SOUTH

Messenger et al., [12]

PALDA5

PALDA5

Didelphis albiventris

Argentina

Chaco

-27.133

-61.460

2001

SOUTH

Messenger et al., [12]

PALDAV2

PALDAV2^3

Triatoma infestans

Argentina

Chaco

-27.133

-61.460

2001

SOUTH

Messenger et al., [12]

PALDA20

PALDA20

Didelphis albiventris

Argentina

Chaco

-27.133

-61.460

2001

SOUTH

Messenger et al., [12]

COTMA38

COTMA38

Akodon boliviensis

Bolivia

Cotopachi

-17.430

-66.270

2004

SOUTH

Messenger et al., [12]

P234

P234

Homo sapiens

Bolivia

Cochabamba

-17.380

-66.160

1985

SOUTH

Messenger et al., [12]

P238

P238

Homo sapiens

Bolivia

Cochabamba

-17.380

-66.160

1985

SOUTH

Messenger et al., [12]

P268

P268

Homo sapiens

Bolivia

Cochabamba

-17.380

-66.160

1987

SOUTH

Messenger et al., [12]

SJM22

SJM22 cl1

Didelphis marsupialis

Bolivia

Beni

-14.810

-64.600

2004

SOUTH

Messenger et al., [12]

SJM34

SJM34

Didelphis marsupialis

Bolivia

Beni

-14.810

-64.600

2004

SOUTH

Messenger et al., [12]

SJM37

SJM37

Didelphis marsupialis

Bolivia

Beni

-14.810

-64.600

2004

SOUTH

Messenger et al., [12]

SJM39

SJM39 cl3

Didelphis marsupialis

Bolivia

Beni

-14.810

-64.600

2004

SOUTH

Messenger et al., [12]

SJM41

SJM41

Philander opossum

Bolivia

Beni

-14.810

-64.600

2004

SOUTH

Messenger et al., [12]

SJMC12

SJMC12

Philander opossum

Bolivia

Beni

-14.810

-64.600

2004

SOUTH

Messenger et al., [12]

XE5167

XE5167 cl1

Didelphis marsupialis

Brasil

Para

-1.710

-48.880

1999

SOUTH

Messenger et al., [12]

IM4810

IM4810

Didelphis marsupialis

Brasil

Manaus

-3.070

-60.160

2002

SOUTH

Messenger et al., [12]

B2085

B2085

Didelphis marsupialis

Brasil

Belem

-1.360

-48.360

1991

SOUTH

Messenger et al., [12]

XE2929

XE2929

Didelphis marsupialis

Brasil

Pará

-5.830

-48.030

1988

SOUTH

Messenger et al., [12]

AAA1cl5

AAA1cl5

Rhodnius prolixus

Colombia

Casanare

4.150

-71.200

2010

SOUTH

Ramirez et al., Molecular Ecology In press

AAA7cl2

AAA7cl2

Rhodnius prolixus

Colombia

Casanare

5.100

-71.600

2010

SOUTH

Ramirez et al., Molecular Ecology In press

AAB3cl3

AAB3cl3

Rhodnius prolixus

Colombia

Casanare

4.150

-71.200

2010

SOUTH

Ramirez et al., Molecular Ecology In press

AAC1cl3

AAC1cl3

Rhodnius prolixus

Colombia

Casanare

5.100

-71.600

2010

SOUTH

Ramirez et al., Molecular Ecology In press

AACf1cl4

AACf1cl4

Canis familiaris

Colombia

Casanare

5.100

-71.600

2010

SOUTH

Ramirez et al., Molecular Ecology In press

AAD6cl6

AAD6cl6

Rhodnius prolixus

Colombia

Casanare

5.100

-71.600

2010

SOUTH

Ramirez et al., Molecular Ecology In press

CACQcl7

CACQcl7

Homo sapiens

Colombia

Santander

6.963

-73.420

2009

TcIDOM

Ramirez et al., Molecular Ecology In press

CACQcl8

CACQcl8

Homo sapiens

Colombia

Santander

6.644

-73.654

2009

TcIDOM

Ramirez et al., Molecular Ecology In press

DYRcl16

DYRcl16

Homo sapiens

Colombia

Boyacá

5.640

-72.899

2007

TcIDOM

Ramirez et al., Molecular Ecology In press

EBcl11

EBcl11

Homo sapiens

Colombia

Boyacá

5.130

-73.119

2007

TcIDOM

Ramirez et al., Molecular Ecology In press

FECcl10

FECcl10

Homo sapiens

Colombia

Boyacá

5.920

-73.500

2001

TcIDOM

Ramirez et al., Molecular Ecology In press

Td3cl11

Td3cl11

Triatoma dimidiata

Colombia

Boyacá

6.270

-71.200

2000

TcIDOM

Ramirez et al., Molecular Ecology In press

X-1084cl10

X-1084cl10

Rhodnius prolixus

Colombia

Boyacá

4.960

-73.630

2010

SOUTH

Ramirez et al., Molecular Ecology In press

X-236cl9

X-236cl9

Rhodnius prolixus

Colombia

Boyacá

4.960

-73.630

2010

SOUTH

Ramirez et al., Molecular Ecology In press

YAS1cl3

YAS1cl3

Alouatta spp

Colombia

Casanare

5.300

-72.400

2010

SOUTH

Ramirez et al., Molecular Ecology In press

38

38

Triatoma dimidiata

Guatemala

Jutiapa

14.287

-89.844

2000

NORTH-CENT

This study

46

46

Triatoma dimidiata

Guatemala

Santa Rosa

14.177

-90.303

2001

NORTH-CENT

This study

66

66

Triatoma dimidiata

Guatemala

Jalapa

14.633

-89.989

2001

NORTH-CENT

This study

67

67

Triatoma dimidiata

Guatemala

Jutiapa

14.287

-89.844

2001

NORTH-CENT

This study

70

70

Triatoma dimidiata

Guatemala

Jutiapa

14.287

-89.844

2001

NORTH-CENT

This study

71

71

Triatoma dimidiata

Guatemala

Jalapa

14.633

-89.989

2001

NORTH-CENT

This study

83

83

Triatoma dimidiata

Guatemala

Chiquimula

14.768

-89.458

2002

NORTH-CENT

This study

95

95

Triatoma dimidiata

Guatemala

Chiquimula

14.768

-89.458

2002

NORTH-CENT

This study

100

100

Triatoma dimidiata

Guatemala

Santa Rosa

14.177

-90.303

2002

NORTH-CENT

This study

113

113

Triatoma dimidiata

Guatemala

Chiquimula

14.768

-89.458

2002

NORTH-CENT

This study

116

116

Triatoma dimidiata

Guatemala

Baja Verapaz

15.079

-90.413

2002

NORTH-CENT

This study

154

154

Triatoma dimidiata

Guatemala

Alta Verapaz

15.594

-90.149

2002

NORTH-CENT

This study

DAVIScl1

DAVIS 9.90 cl1

Triatoma dimidiata

Honduras

Tegucigalpa

14.080

-87.200

1983

NORTH-CENT

Messenger et al., 2012

ANITA II

ANITA

Triatoma dimidiata

Mexico

Campeche

19.188

-90.300

2011

NORTH-CENT

This study

CAM6

CAM6

Triatoma dimidiata

Mexico

Campeche

19.188

-90.300

2011

NORTH-CENT

This study

CRISTY

CRISTY

Homo sapiens

Mexico

San Luis Potosí

22.159

-100.990

2007

NORTH-CENT

This study

MICH1

MICH

Triatoma dimidiata

Mexico

Michoacan

19.567

-101.707

2011

NORTH-CENT

This study

NINOA

NINOA

Homo sapiens

Mexico

Oaxaca

17.054

-96.714

1994

NORTH-CENT

This study

PLI

PL

Dipetalogaster maxima

Mexico

Baja California Sur

26.044

-111.666

2001

NORTH-CENT

This study

QROI

QRO

Triatoma barberi

Mexico

Queretaro

20.594

-100.393

1986

NORTH-CENT

This study

TQI

TQ

Triatoma pallidipennis

Mexico

Morelos

18.953

-99.223

1991

NORTH-CENT

This study

XAL1

XAL

Triatoma dimidiata

Mexico

Veracruz

19.173

-96.133

2003

NORTH-CENT

This study

9209802P

9209802P cl1

Didelphis marsupialis

USA

Georgia

32.430

-83.310

1992

NORTH-CENT

Messenger et al., [12]

9307

93070103P cl1

Didelphis marsupialis

USA

Georgia

32.430

-83.310

1993

NORTH-CENT

Messenger et al., [12]

ARMA

USAARMA cl3

Dasypus novemcinctus

USA

Lousiana

30.500

-91.000

Unknown

NORTH-CENT

Messenger et al., [12]

USA

USAOPOSSUM cl2

Didelphis marsupialis

USA

Lousiana

30.500

-91.000

Unknown

NORTH-CENT

Messenger et al., [12]

9354

9354

Homo sapiens

Venezuela

Sucre

10.460

-63.610

1999

TcIDOM

Messenger et al., [12]

11541

11541

Homo sapiens

Venezuela

Merida

8.590

-71.230

2003

TcIDOM

Messenger et al., [12]

11713

11713

Homo sapiens

Venezuela

Lara

10.233

-69.866

2003

TcIDOM

Messenger et al., [12]

11804

11804

Homo sapiens

Venezuela

Portuguesa

9.084

-69.103

2003

TcIDOM

Messenger et al., [12]

10462P2C3

10462P2C3

Homo sapiens

Venezuela

Miranda

10.266

-66.485

Unknown

TcIDOM

This study

10462P2C7

10462P2C7

Homo sapiens

Venezuela

Miranda

10.080

-66.449

Unknown

TcIDOM

This study

10968P1C1

10968P1C1

Homo sapiens

Venezuela

Sucre

10.406

-63.298

Unknown

TcIDOM

This study

ANT3P1C6

ANT3P1C6

Homo sapiens (oral)

Venezuela

DC

10.500

-66.951

Unknown

SOUTH

This study

M13

M13

Didelphis marsupialis

Venezuela

Barinas

7.500

-71.230

2004

SOUTH

Messenger et al., [12]

M16

M16 cl4

Didelphis marsupialis

Venezuela

Barinas

7.500

-71.230

2004

SOUTH

Messenger et al., [12]

M18

M18

Didelphis marsupialis

Venezuela

Barinas

7.500

-71.230

2004

SOUTH

Messenger et al., [12]

M7

M7

Didelphis marsupialis

Venezuela

Barinas

7.500

-71.230

2004

SOUTH

Messenger et al., [12]

92122

92122102R

Procyon lotor

TcIV

USA

Georgia

  

OUTGROUPS

Messenger et al., [12]

CANIII

CANII cl1

Homo sapiens

TcIV

Brazil

Belem

  

OUTGROUPS

Messenger et al., [12]

CM17

CM17

Dasypus spp.

TcIII

Colombia

Carimaga

  

OUTGROUPS

Messenger et al., [12]

X1060

X10610 cl5

Homo sapiens

TcIV

Venezuela

Guárico

  

OUTGROUPS

Messenger et al., [12]

ERA

ERA cl2

Homo sapiens

TcIV

Venezuela

Anzoátegui

  

OUTGROUPS

Messenger et al., [12]

10R26

10R26

Aotus spp.

TcIV

Bolivia

Santa Cruz

  

OUTGROUPS

Messenger et al., [12]

SAIRI3

Saimiri3 cl1

Saimiri sciureus

TcIV

Venezuela

Venezuela

  

OUTGROUPS

Messenger et al., [12]

Isolates from México and Guatemala were characterized to DTU level via the amplification and sequencing of glucose-6-phosphate isomerase (GPI) as previously described by Lauthier et al., (2012)[18]. Subsequently, nine maxicircle gene fragments were amplified, sequenced and concatenated from the Méxican and Guatemalan strains according to Messenger et al., 2012 (excluding ND4)[12]. Phylogenetic analysis was also conducted as in Messenger et al., 2012[12]. Nineteen nuclear microsatellite loci previously described by Llewellyn et al., 2009[13], were selected based on their level of TcI intra-lineage resolution. Microsatellite loci were amplified across 21 unpublished biological stocks from México and Guatemala. Reaction conditions were as described previously[13]. Dendrograms based on multilocus allele profiles were constructed also according to Llewellyn et al., 2009[13].

Maxicircle nucleotide diversity (π) was calculated for TcINORTH-CENT, TcISOUTH and TcIDOM respectively in DNAsp v5[19]. Nuclear allelic diversity was calculated for the same populations using allelic richness (Ar) in FSTAT[20]. The resulting values are shown in Figure1.
Figure 1

Nucleotide diversity and allelic richness comparisons across North and South American. Trypanosoma cruzi I populations. Left hand data points (diamond) indicate allelic richness ± standard error over loci. Right hand data points (square) indicate nucleotide diversity (π) ± standard error over pair-wise comparisons.

Nucleotide sequences per gene fragment are available from GenBank under the accession numbers MURF1 (fragment a): JX431060 - JX431084; MURF1 (fragment b): JX431085 - JX431109; ND1: JX431110 - JX431134; ND5 (fragment a): JX431135 - JX431159; ND5 (fragment b): JX431160 - JX431184; 9S rRNA: JX431185 - JX431209; 12S rRNA: JX431210 - JX431234; COII: JX431235 - JX431259 and CYT b: JX431260 - JX431284.

Across the 3,449 bp final concatenated alignment (including outgroups), a total of 374 variable sites were found. The mitochondrial phylogeny supported the presence of significant diversity among the isolates examined (Figure2). TcIDOM strains formed a monophyletic clade [60% ML BS/0.98 BPP]. The principal division in the phylogeny was between TcISOUTH and TcIDOM/TcINORTH-CENT (98% ML BS/0.98 BPP). However, this division is incomplete, such that a subset of South American strains is also grouped with TcIDOM and TcINORTH-CENT. Thus, it is not possible to conclude that TcIDOM maxicircle sequences nest uniquely among those from TcINORTH-CENT strains. Conversely, a basal relationship of the TcINORTH-CENT to TcIDOM is suggested at the level of nucleotide diversity by population (Figure1), whereby TcIDOM<TcINORTH-CENT<TcISOUTH. Low standard errors about the mean in all three populations, but especially in TcIDOM and TcINORTH-CENT, suggest that sample size had little impact on the accuracy of estimation between populations.
Figure 2

Isolate grouping of 72 Trypanosoma cruzi I strains, as well as outgroups, based on nine concatenated maxicircle sequences. Bayesian consensus topology is displayed. Bayesian posterior probability analysis (BPP) was performed using MrBAYES v3.1. Five independent analyses were run using a random starting tree with three heated chains and one cold chain over 10 million generations with sampling every 10 simulations (25% burn-in). Decimal values (second number) on nodes indicate Bayesian probabilities for clusters. First number indicates the Maximum-Likelihood (ML) % bootstrap support for clade topologies, which was estimated following the generation of 1000 pseudo-replicate datasets. Branch colours indicate isolate origin. Isolates that show clear incongruity between nuclear genotype and maxicircle genotype are marked. Outgroup branches were cropped for ease of visualization, full branch lengths are show inset top right.

Distance-based clustering using the microsatellite dataset indicated the presence of several well defined clades (Figure3). Importantly in this case the monophyly of North-Central American isolates was corroborated, and TcIDOM clustered firmly within them (bootstrap 65%). By contrast, South American isolates fall into a divergent but diverse clade. Thus the nuclear data provide stronger support for divergence of TcIDOM from within TcINORTH-CENT than the maxicircle phylogeny. Sample size-corrected allelic richness estimates are consistent with hierarchical patterns of clustering based on pair-wise genetic distances. As with the maxicircle dataset, there is a pronounced cline in diversity across the populations studied - Ar TcIDOM< Ar TcINORTH-CENT< Ar TcISouth (Figure1).
Figure 3

Isolate grouping of 72 Trypanosoma cruzi I strains based on nineteen nuclear micrsoatellite markers. Neighour-joining clustering algorithm implemented. Bootstrap values are included on important nodes. The first figure indicates % bootstrap support over 10,000 trees, the second the % stability over 1000 trees accounting for multi-allelic loci in the dataset. For further details see Llewellyn et al., 2009[13]. Branch colours indicate isolate origin. The three principal populations TcIDOM TcISOUTH and TcINORTH-CENT are shown on both map and tree. Red circles correspond to isolates from TcIDOM. Isolates that show clear incongruity between nuclear genotype and maxicircle genotype are marked with reference to Figure2.

TcI dispersion into Central and North America

Using a 100 MYA biogeographic calibration point[6], molecular clock analyses point to the origin of T. cruzi (sensu stricto) 5 – 1 MYA[2123] and a most recent common ancestor for TcI at 1.3-0.2 MYA[22]. Reduced genetic diversity among North-Central American isolates by comparison to their southern counterparts is powerful evidence in support of others who suggest that TcI originated in South America[13, 24]. The emergence of TcI in the South occurred prior to either migration across the Isthmus of Panama alongside didelphid marsupials during the Great American Interchange[25], or perhaps prior to northerly dispersal via volant mammals (e.g. bats).

Origin of TcIDOM

Recent findings indicate a close resemblance between TcIDOM isolates from the northern region of South America and parasite populations from Central and North America by the use of nuclear and mitochondrial markers[1113]. Indeed SL-IR genotyping suggests a distribution for TcIDOM that now extends as far south as the Argentine Chaco, where multiple sequences have been identified from human and domestic vector sources[14]. Llewellyn et al., (2009) originally hypothesised that a distinct human/domestic clade could be maintained despite the presence of nearby infective sylvatic strains due to the low parasite transmission efficiency by the vector[13]. In this case multiple feeds by domestic vector nymphs are required to infect individuals, as such human – human transmission is far more common than reservoir host - human transmission. Originally this hypothesis was developed to explain the epidemiology of Chagas disease in Venezuela. However, TcIDOM is clearly widespread and recent data propose a date for its emergence 23,000 ± 12,000 years ago[11]. This corresponds to the earliest human colonisation of the Americas[26]. Thus it seems that TcIDOM may be as ancient as humans in South America. Crucially, our data, which show that TcIDOM is nested among North and Central American strains, suggest that this widespread domestic T. cruzi genotype may actually have made first contact with man in North–Central America.

The expansion of limited diversity genotypes into domestic transmission cycles is a familiar story in T. cruzi. This phenomenon seems to have occurred almost simultaneously with TcIDOM (<60,000 YA) in the Southern Cone region but involving DTUs TcV and TcVI[22]. Nonetheless, static human population densities sufficient to support a sustained domestic cycle are presumably vital. For TcIDOM, patterns of genetic diversity suggest early colonizing Amerindians may have been responsible for its southerly migration and dispersal from North/Central America. However, such early settler populations were probably small, dynamic, and inherently unsuitable to sustain transmission of such a genotype. Many questions, therefore, remain unanswered regarding its emergence. Insight could perhaps be drawn from a better understanding of the current distribution and diversity of TcIDOM (including samples from the Southern Cone), patterns of vector population migrations, and even from analysis of ancient DNA (e.g.[27]). We hope this report serves to galvanize efforts towards this understanding, especially among researchers in Central and North America, where many of the answers lie.

Declarations

Acknowledgements

FZE received an MSc scholarship from the Méxican Council of Science and Technology (CONACyT), and financial support from the International Agency of National Public Health Institutes. LAM, MDL, MAM and MSL acknowledge support from the European FP7 Project ChagasEpiNet, Grant 223034. MSL would like to thank Juan David Ramirez and Prof. Felipe Guhl at the Universidad de los Andes, Colombia for constructive discussion.

Authors’ Affiliations

(1)
Centro Regional de Investigación en Salud Pública, Instituto Nacional de Salud Pública
(2)
London School of Hygiene and Tropical Medicine
(3)
Department of Biology, University of Maryland
(4)
Área de Entomología Médica, Centro Universitario del Sur, Universidad de Guadalajara
(5)
Center for Health Studies, Research Institute, Universidad del Valle de Guatemala
(6)
Instituto de Medicina Tropical, Universidad Central de Venezuela

References

  1. Rassi A, Rassi A, Marin-Neto JA: Chagas disease. Lancet. 2010, 375 (9723): 1388-1402. 10.1016/S0140-6736(10)60061-X.View ArticlePubMedGoogle Scholar
  2. Carlier Y, Torrico F, Sosa-Estnai S, Russomando G, Luquetti A, Frelij H, Albajar Vinas P: Congenital chagas disease: recommendations for diagnosis, treatment and control of newborns, siblings and pregnant women. PLoS Negl Trop Dis. 2011, 5: e1250-10.1371/journal.pntd.0001250.PubMed CentralView ArticlePubMedGoogle Scholar
  3. Alarconde Noya B, Diaz-Bello Z, Colmenares C, Ruiz-Guevara R, Mauriello L, Zavala-Jaspe R, Suarez JA, Abate T, Naranjo L, Paiva M, Rivas L, Castro J, Marques J, Mendoza I, Acquatella H, Torres J, Noya O: Large urban outbreak of orally acquired acute Chagas disease at a school in Caracas, Venezuela. J Infect Dis. 2010, 201 (9): 1308-1315. 10.1086/651608.View ArticlePubMedGoogle Scholar
  4. Lima L, Silva FM, Neves L, Attias M, Takata CS, Campaner M, de Souza W, Hamilton PB, Teixeira MM: Evolutionary Insights from Bat Trypanosomes: Morphological, Developmental and Phylogenetic Evidence of a New Species, Trypanosoma (Schizotrypanum) erneyi sp. nov., in African Bats Closely Related to Trypanosoma (Schizotrypanum) cruzi and Allied Species. Protist. 2012, 163: 856-872. 10.1016/j.protis.2011.12.003.View ArticlePubMedGoogle Scholar
  5. Hamilton PB, Stevens JR, Gaunt MW, Gidley J, Gibson WC: Trypanosomes are monophyletic: evidence from genes for glyceraldehyde phosphate dehydrogenase and small subunit ribosomal RNA. Int J Parasitol. 2004, 34 (12): 1393-1404. 10.1016/j.ijpara.2004.08.011.View ArticlePubMedGoogle Scholar
  6. Stevens JR, Noyes HA, Dover GA, Gibson WC: The ancient and divergent origins of the human pathogenic trypanosomes. Trypanosoma brucei and T. cruzi. Parasitology. 1999, 118 (Pt 1): 107-116.PubMedGoogle Scholar
  7. Hamilton PB, Teixeira MM, Stevens JR: The evolution of Trypanosoma cruzi: the 'bat seeding' hypothesis. Trends Parasitol. 2012, 28 (4): 136-141. 10.1016/j.pt.2012.01.006.View ArticlePubMedGoogle Scholar
  8. Yeo M, Acosta N, Llewellyn M, Sanchez H, Adamson S, Miles GA, Lopez E, Gonzalez N, Patterson JS, Gaunt MW, de Arias AR, Miles MA: Origins of Chagas disease: Didelphis species are natural hosts of Trypanosoma cruzi I and armadillos hosts of Trypanosoma cruzi II, including hybrids. Int J Parasitol. 2005, 35 (2): 225-233. 10.1016/j.ijpara.2004.10.024.View ArticlePubMedGoogle Scholar
  9. Zingales B, Andrade SG, Briones MR, Campbell DA, Chiari E, Fernandes O, Guhl F, Lages-Silva E, Macedo AM, Machado CR, Miles MA, Romanha AJ, Sturm NR, Tibayrenc M, Schijman AG: A new consensus for Trypanosoma cruzi intraspecific nomenclature: second revision meeting recommends TcI to TcVI. Mem Inst Oswaldo Cruz. 2009, 104 (7): 1051-1054. 10.1590/S0074-02762009000700021.View ArticlePubMedGoogle Scholar
  10. Miles MA, Llewellyn MS, Lewis MD, Yeo M, Baleela R, Fitzpatrick S, Gaunt MW, Mauricio IL: The molecular epidemiology and phylogeography of Trypanosoma cruzi and parallel research on Leishmania: looking back and to the future. Parasitology. 2009, 136 (12): 1509-1528. 10.1017/S0031182009990977.View ArticlePubMedGoogle Scholar
  11. Ramírez J, Guhl F, Messenger L, Lewis M, Montilla M, Cucunuba Z, Miles M, Llewellyn M: Contemporary cryptic sexuality in Trypanosoma cruzi. Mol Ecol. 2012, 21: 4216-26. 10.1111/j.1365-294X.2012.05699.x.View ArticlePubMedGoogle Scholar
  12. Messenger LA, Llewellyn MS, Bhattacharyya T, Franzen O, Lewis MD, Ramirez JD, Carrasco HJ, Andersson B, Miles MA: Multiple mitochondrial introgression events and heteroplasmy in Trypanosoma cruzi revealed by maxicircle MLST and next generation sequencing. PLoS Negl Trop Dis. 2012, 6 (4): e1584-10.1371/journal.pntd.0001584.PubMed CentralView ArticlePubMedGoogle Scholar
  13. Llewellyn MS, Miles MA, Carrasco HJ, Lewis MD, Yeo M, Vargas J, Torrico F, Diosque P, Valente V, Valente SA, Gaunt MW: Genome-scale multilocus microsatellite typing of Trypanosoma cruzi discrete typing unit I reveals phylogeographic structure and specific genotypes linked to human infection. PLoS Pathog. 2009, 5 (5): e1000410-10.1371/journal.ppat.1000410.PubMed CentralView ArticlePubMedGoogle Scholar
  14. Cura CI, Mejia-Jaramillo AM, Duffy T, Burgos JM, Rodriguero M, Cardinal MV, Kjos S, Gurgel-Goncalves R, Blanchet D, De Pablos LM, Tomasini N, da Silva A, Russomando G, Cuba CA, Aznar C, Abate T, Levin MJ, Osuna A, Gurtler RE, Diosque P: Trypanosoma cruzi I genotypes in different geographical regions and transmission cycles based on a microsatellite motif of the intergenic spacer of spliced-leader genes. Int J Parasitol. 2010, 40 (14): 1599-1607. 10.1016/j.ijpara.2010.06.006.PubMed CentralView ArticlePubMedGoogle Scholar
  15. Pennington PM, Paiz C, Grajeda LM, Cordon-Rosales C: Short report: concurrent detection of Trypanosoma cruzi lineages I and II in domestic Triatoma dimidiata from Guatemala. Am J Trop Med Hyg. 2009, 80 (2): 239-241.PubMedGoogle Scholar
  16. Bucio MI, Cabrera M, Segura EL, Zenteno E, Salazar-Schettino M: Identification of immunodominant antigens in Mexican strains of Trypanosoma cruzi. Immunol Invest. 1999, 28 (4): 257-268. 10.3109/08820139909060860.View ArticlePubMedGoogle Scholar
  17. Herrera C, Bargues MD, Fajardo A, Montilla M, Triana O, Vallejo GA, Guhl F: Identifying four Trypanosoma cruzi I isolate haplotypes from different geographic regions in Colombia. Infect Genet Evol. 2007, 7 (4): 535-539. 10.1016/j.meegid.2006.12.003.View ArticlePubMedGoogle Scholar
  18. Lauthier JJ, Tomasini N, Barnabe C, Rumi MM, D'Amato AM, Ragone PG, Yeo M, Lewis MD, Llewellyn MS, Basombrio MA, Miles MA, Tibayrenc M, Diosque P: Candidate targets for Multilocus Sequence Typing of Trypanosoma cruzi: validation using parasite stocks from the Chaco Region and a set of reference strains. Infect Genet Evol. 2012, 12 (2): 350-358. 10.1016/j.meegid.2011.12.008.View ArticlePubMedGoogle Scholar
  19. Librado P, Rozas J: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009, 25 (11): 1451-1452. 10.1093/bioinformatics/btp187.View ArticlePubMedGoogle Scholar
  20. Goudet J: FSTAT Version 1.2: a computer program to calculate F-statistics. J Heredity. 1995, 86: 485-486.Google Scholar
  21. Flores-Lopez CA, Machado CA: Analyses of 32 loci clarify phylogenetic relationships among Trypanosoma cruzi lineages and support a single hybridization prior to human contact. PLoS Negl Trop Dis. 2011, 5 (8): e1272-10.1371/journal.pntd.0001272.PubMed CentralView ArticlePubMedGoogle Scholar
  22. Lewis MD, Llewellyn MS, Yeo M, Acosta N, Gaunt MW, Miles MA: Recent, Independent and Anthropogenic Origins of Trypanosoma cruzi Hybrids. PLoS Negl Trop Dis. 2011, 5 (10): e1363-10.1371/journal.pntd.0001363.PubMed CentralView ArticlePubMedGoogle Scholar
  23. Machado CA, Ayala FJ: Nucleotide sequences provide evidence of genetic exchange among distantly related lineages of Trypanosoma cruzi. Proc Natl Acad Sci U S A. 2001, 98 (13): 7396-7401. 10.1073/pnas.121187198.PubMed CentralView ArticlePubMedGoogle Scholar
  24. Barnabe C, Yaeger R, Pung O, Tibayrenc M: Trypanosoma cruzi: a considerable phylogenetic divergence indicates that the agent of Chagas disease is indigenous to the native fauna of the United States. Exp Parasitol. 2001, 99 (2): 73-79. 10.1006/expr.2001.4651.View ArticlePubMedGoogle Scholar
  25. Marshall LG, Sempere T: Evolution of the neotropical Cenozoic land mammal fauna in its geochronologic, stratigraphic, and tectonic context. Biological relationships between Africa and South America. Edited by: Goldblatt P. 1993, Yale University Press, New Haven, 329-392.Google Scholar
  26. Goebel T, Waters MR, O'Rourke DH: The late Pleistocene dispersal of modern humans in the Americas. Science. 2008, 319 (5869): 1497-1502. 10.1126/science.1153569.View ArticlePubMedGoogle Scholar
  27. Lima VS, Iniguez AM, Otsuki K, Fernando Ferreira L, Araujo A, Vicente AC, Jansen AM: Chagas disease in ancient hunter-gatherer population, Brazil. Emerg Infect Diseases. 2008, 14 (6): 1001-1002. 10.3201/eid1406.0707.View ArticleGoogle Scholar

Copyright

© Zumaya-Estrada et al.; licensee BioMed Central Ltd. 2012

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Advertisement