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Molecular Population Genetics and Phylogeography of the Chagas Disease Vector Triatoma infestans in South America

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R V Piccinali
R V Piccinali
R V Piccinali
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Paula L Marcet at Centers for Disease Control and Prevention
Paula L Marcet
François Noireau
François Noireau
François Noireau
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U Kitron
U Kitron
U Kitron
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Knowledge of the genetic variability, population structure, and evolutionary history of Triatoma infestans may be useful for developing rational vector control strategies. A 661-bp fragment of the mitochondrial gene cytochrome oxidase I (COI) was sequenced and analyzed in bugs from Argentina, Uruguay, Peru, and Bolivia, including peridomestic, domestic, Andean, and Chaco sylvatic bugs. A total of 48 polymorphic sites among 37 haplotypes were described. Nucleotide variation fluctuated among samples, with the highest nucleotide diversity observed in seven Argentinean provinces. Within this group, some populations showed patterns of variability compatible with population expansions and/or fine-scale population structure, whereas others suggested population bottlenecks and/or population admixture processes. A maximum parsimony analysis of the haplotypes showed the presence of a Bolivian/Peruvian and an Argentinean/Uruguayan clade. Bolivian sequences were further divided in Chaco sylvatic and Andean domestic and sylvatic. Two different nested clades were found within the Argentinean/Uruguayan cluster. Analysis of molecular variance (AMOVA) and K(ST)* analysis supported a strong population structure in Argentina, where genetic differentiation was correlated with geographic distance. Departures from neutrality expectations and a nested cladistic analysis suggest a recent population expansion of T. infestans in Argentina, followed by restricted gene flow and patterns of isolation by distance. This expansion could have taken place as a two-wave process, as was shown by the phylogenetic analysis and signatures of population admixture in the southern most Argentinean populations.
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Molecular Population Genetics and Phylogeography of the Chagas Disease Vector Triatoma infestans in South Ameri
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... Levels of genetic diversity in most of the insecticide-treated localities were similar or higher than in untreated areas and no bottlenecks effects were detected, suggesting a limited effect of spraying erasing genetic variability. A latter study [31] confirmed several of these patterns and proposed, as in a previous study based on the mtCOI gene [32], the existence of two colonization events of T. infestans in Argentina, one dispersal line through the Andes and the other from non-Andean lowlands. ...
Triatoma infestans (Hemiptera: Reduviidae) Population Genetics: What Have We Learned from Microsatellites?
Article
Full-text available
  • Feb 2024
Purpose of Review The genetic structure of insect vectors offers valuable insights for identifying panmictic units, reinfestation sources, and minimal intervention units in vector control programs. This review highlights key findings on the genetic structure of Triatoma infestans populations using microsatellites across various geographic scales and landscapes. Recent Findings Microsatellites have been employed to explore the genetic structure of T. infestans across Argentina, Bolivia, Paraguay, Brazil, and Peru. Research has focused on understanding genetic structure, assessing the impacts of short and long-distance migration, identifying sources of reinfestation post-insecticide spraying, evaluating the effects of insecticides on variability, and investigating the potential contribution of sylvatic foci to household infestation. Summary Triatoma infestans populations are highly structured across countries, landscapes, and geographical levels. Although support for the isolation-by-distance migration model is mixed, most studies point to a combination of active and passive dispersal. Insecticide spraying significantly influences genetic structure, intensifying differentiation. Reinfestation is mainly attributed to internal residual foci at the village level. Finally, the contribution of sylvatic populations to (re)infestation varies across geographic areas. Graphical Abstract
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... Similarly, populations from southern Brazil show greater morphometric proximity to populations from Argentina. The proximity of the border between the southern region of Brazil and Argentina is related to dispersion through the Argentinean Gran Chaco, as suggested by Piccinali et al. (2011) [10,11] and Waleckx et al. (2011) [9]. Even if our data do not support the hypothesis, the proximity between populations is demonstrated in this study. ...
Characterization of Triatoma infestans (Klug, 1834) (Hemiptera: Heteroptera, Reduviidae) from Residual Foci in the States of Bahia and Rio Grande do Sul, Brazil, Using Geometric Morphology
Article
Full-text available
  • Mar 2023
Triatoma infestans is one of the main vectors of Chagas disease in Latin America. Although the species is under control in most Latin countries, it is still necessary to maintain epidemiological surveillance. The present study aims to characterize T. infestans populations from residual foci in Bahia and Rio Grande do Sul, Brazil, comparing them with natural populations in Argentina and Bolivia. For this, we adopt the geometric morphometry of the heads. It is possible to report the morphometric variety of the studied populations. In addition, we show that the size of the heads contributes to the differentiation between populations, while the shape has less power to discriminate groups. Furthermore, we show that some natural populations have morphometric proximity to residual populations, suggesting a relationship between these triatomines. Our data do not support the origin of residual populations but demonstrate the importance of new studies with other techniques to understand the dynamics of distribution and reintroduction of these vectors in Brazilian territory.
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... Among them, Triatoma infestans (Klug) is the main vector of T. cruzi in the Southern Cone of Latin America between latitudes 10°S and 46°S. Across its distribution, T. infestans is primarily restricted to domestic and peridomestic environments, such as human dwellings, chicken coops, and pig or goat corrals (Abalos 1974;Schofield 1985;Schofield and Dolling 1993 Mitochondrial DNA gene fragments have been used in a number of T. infestans population genetic analyses; however, the maternally inherited markers analyzed until the present exhibited low or limited levels of variation (Giordano et al. 2005;Piccinali et al. 2009;García et al. 2013;Fernández et al. 2013Fernández et al. , 2020. Comparative analysis of the complete mitochondrial genome (mitogenome) among individuals of this species would be potentially useful in studies on the evolutionary history and populations of the vector. ...
Variation in the Mitochondrial Genome of the Chagas Disease Vector Triatoma infestans (Hemiptera: Reduviidae)
Article
  • Mar 2022
  • NEOTROP ENTOMOL
Chagas' disease is transmitted mainly by members of the subfamily Triatominae (Hemiptera: Reduviidae). Among them, Triatoma infestans (Klug) is the main vector of the disease in Southern Cone of Latin America. In order to contribute to knowledge of the genetic variation between triatomine vectors, in the present study, we analyzed the intraspecific and interspecific variations of the seven mitogenomes available from Triatominae. In addition, in order to examine their evolutionary relationships with others species of Reduviidae and to estimate the divergence time of the main lineages, we constructed phylogenetic trees including mitogenome sequences of 30 species from Reduviidae. Comparative analysis between mitochondrial DNA sequences from two specimens of T. infestans revealed a total of 54 variable sites. Triatoma infestans, Triatoma dimidiata (Latreille), Triatoma rubrofasciata (De Geer), Triatoma migrans (Breddin), Rhodnius pictipes (Stål), and Panstrongylus rufotuberculatus (Champion) present similar mitogenome organization and the length differences observed among these species are primarily caused by variations in control region (CR) and intergenic spacers (IGS). The relative synonymous codon usage values (RSCU) were similar in the six species of Triatominae, and in agreement with the observed in other insects, a biased use of A and C nucleotides in the majority strand was detected. The monophyly of five subfamilies was strongly supported (Phymatinae, Peiratinae, Triatominae, Stenopodainae, and Harpactorinae), while the sampled species of Reduviinae were grouped with one specie from the Salyavatinae subfamily. The oldest subfamily is Phymatinae at 100.3 Mya (99.6-102.2 Mya) and the youngest is Triatominae and Stenopodainae at 52.6 Mya (42.5-63.7 Mya). The estimated diversification time for the Triatominae subfamily agrees with the Andean uplift geological event. An analysis with more mitogenomes from more Triatominae species would be necessary to provide sufficient evidence to support this finding.
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... En todas estas aproximaciones, el conocimiento sobre la diversidad y estructura genética es una herramienta fundamental para inferir tendencias y hacer predicciones sobre la dinámica de los vectores y potencialmente de los patógenos (Piccinali et al. 2009). Con esta información, los tomadores de decisiones sobre el control de vectores cuentan con más y mejores elementos para aplicar programas de control que pueden diferir de una localidad a otra. ...
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... In this study, the elevated genetic diversity of both Mat populations could represent the assemblage of individuals from distinct genetic units, as they have been under higher selective pressure than the sylvatic populations from 20oct, KM and Ili, located further away from the domestic area subjected to vector control. High levels of genetic diversity have also been reported in several domestic non-Andean T. infestans populations from the Gran-Chaco area (Perez de Rosas et al., 2013;Piccinali et al., 2009), of which many had been subject to extensive vector control pressure. ...
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... In this study, the elevated genetic diversity of both Mat populations could represent the assemblage of individuals from distinct genetic units, as they have been under higher selective pressure than the sylvatic populations from 20oct, KM and Ili, located further away from the domestic area subjected to vector control. High levels of genetic diversity have also been reported in several domestic non-Andean T. infestans populations from the Gran-Chaco area (Perez de Rosas et al., 2013;Piccinali et al., 2009), of which many had been subject to extensive vector control pressure. ...
Insights into the evolution and dispersion of pyrethroid resistance among sylvatic Andean Triatoma infestans from Bolivia
Article
  • Feb 2021
  • INFECT GENET EVOL
Sylvatic populations of Triatoma infestans represent a challenge to Chagas disease control as they are not targeted by vector control activities and may play a key role in post-spraying house re-infestation. Understanding sylvatic foci distribution and gene flow between sylvatic and domestic populations is crucial to optimize vector control interventions and elucidate the development and spread of insecticide resistance. Herein, the genetic profiles of five Andean T. infestans populations from Bolivia with distinct insecticide susceptibility profiles were compared. Multilocus genotypes based on eight microsatellites and the DNA sequence of a fragment of the cytochrome B (cytB) gene were obtained for 92 individuals. CytB haplotypes were analyzed with previously reported Bolivian T. infestans haplotypes to evaluate putative historical gene flow among populations. Each specimen was also screened for two nucleotide mutations in the sodium channel gene (kdr), related to pyrethroid resistance (L1014 and L9251). Significant genetic differentiation was observed among all populations, although individuals of admixed origin were detected in four of them. Notably, the genetic profiles of adjacent domestic and sylvatic populations of Mataral, characterized by higher levels of insecticide resistance, support their common ancestry. Only one sylvatic individual from Mataral carried the kdr mutation L1014, suggesting that this mechanism is unlikely to cause the altered insecticide susceptibility observed in these populations. However, as the resistance mutation is present in the area, it has the potential to be selected under insecticidal pressure. Genetic comparisons of these populations suggest that insecticide resistance is likely conferred by ancient trait(s) in T. infestans sylvatic populations, which are capable of invading domiciles. These results emphasize the need for stronger entomological surveillance in the region, including early detection of house invasion, particularly post-spraying, monitoring for resistance to pyrethroids and the design of integrative control actions that consider sylvatic foci around domestic settings and their dispersion dynamics.
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... The genetic structure of T. infestans at macrogeographic scales adjusts to an isolation-by-distance model (Perez de Rosas et al. 2007Piccinali et al. 2009), while at shorter distances, a hierarchical island model was used to explain the distribution of genetic variability (Piccinali and Gürtler 2015). This picture can be variable among localities and is often affected by pesticide treatment history (Perez de Rosas et al. 2007;Gourbiere et al. 2012). ...
Genetic structure of deltamethrin-resistant populations of Triatoma infestans (Hemiptera: Reduviidae) in the Gran Chaco
Article
Full-text available
  • Oct 2020
  • Parasitol Res
The genetic structure of natural populations offers insight into the complexities of their dynamics, information that can be relevant to vector control strategies. Microsatellites are useful neutral markers to investigate the genetic structure and gene flow in Triatoma infestans, one of the main vectors of Chagas disease in South America. Recently, a heterogeneous pyrethroid-resistant hotspot was found in the Argentine Gran Chaco, characterized by the highest levels of deltamethrin resistance found at the present time. We applied population genetics analyses to microsatellite and village data and search for associations between the genetic variability and the heterogeneous toxicological pattern previously found. We genotyped 10 microsatellite loci in 67 T. infestans from 6 villages with no, low, and high pyrethroid resistance. The most genetically diverse populations were those susceptible or with low values of resistance. In contrast, high-resistance populations had lower herozygosity and some monomorphic loci. A negative association was found between variability and resistant ratios. Global and pairwise FSTs indicated significant differentiation between populations. The only susceptible population was discriminated in all the performed studies. Low-resistance populations were also differentiated by a discriminant analysis of principal components (DAPC) and were composed mostly by the same two genetic clusters according to STRUCTURE Bayesian algorithm. Individuals from the high-resistance populations were overlapped in the DAPC and shared significant proportions of a genetic cluster. These observations suggest that the resistant populations might have a common origin, although more genetic markers and samples are required to test this hypothesis more rigorously.
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Estimating the genetic structure of Triatoma dimidiata (Hemiptera: Reduviidae) and the transmission dynamics of Trypanosoma cruzi in Boyacá, eastern Colombia
Article
Full-text available
  • Jul 2022
Chagas disease is considered a public health issue in Colombia, where many regions are endemic. Triatoma dimidiata is an important vector after Rhodnius prolixus , and it is gaining importance in Boyacá, eastern Colombia. Following the recent elimination of R . prolixus in the region, it is pivotal to understand the behavior of T . dimidiata and the transmission dynamics of T . cruzi . We used qPCR and Next Generation Sequencing (NGS) to evaluate T . cruzi infection, parasite load, feeding profiles, and T . cruzi genotyping for T . dimidiata specimens collected in nine municipalities in Boyacá and explored T . dimidiata population genetics. We found that T . dimidiata populations are composed by a single population with similar genetic characteristics that present infection rates up to 70%, high parasite loads up to 1.46 × 10 ⁹ parasite-equivalents/mL, a feeding behavior that comprises at least 17 domestic, synanthropic and sylvatic species, and a wide diversity of TcI genotypes even within a single specimen. These results imply that T . dimidiata behavior is similar to other successful vectors, having a wide variety of blood sources and contributing to the circulation of different genotypes of the parasite, highlighting its importance for T . cruzi transmission and risk for humans. In the light of the elimination of R . prolixus in Boyacá and the results we found, we suggest that T . dimidiata should become a new target for vector control programs. We hope this study provides enough information to enhance surveillance programs and a future effective interruption of T . cruzi vector transmission in endemic regions.
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Population genomics and geographic dispersal in Chagas disease vectors: Landscape drivers and evidence of possible adaptation to the domestic setting
Article
Full-text available
Accurate prediction of vectors dispersal, as well as identification of adaptations that allow blood-feeding vectors to thrive in built environments, are a basis for effective disease control. Here we adopted a landscape genomics approach to assay gene flow, possible local adaptation, and drivers of population structure in Rhodnius ecuadoriensis , an important vector of Chagas disease. We used a reduced-representation sequencing technique (2b-RADseq) to obtain 2,552 SNP markers across 272 R . ecuadoriensis samples from 25 collection sites in southern Ecuador. Evidence of high and directional gene flow between seven wild and domestic population pairs across our study site indicates insecticide-based control will be hindered by repeated re-infestation of houses from the forest. Preliminary genome scans across multiple population pairs revealed shared outlier loci potentially consistent with local adaptation to the domestic setting, which we mapped to genes involved with embryogenesis and saliva production. Landscape genomic models showed elevation is a key barrier to R . ecuadoriensis dispersal. Together our results shed early light on the genomic adaptation in triatomine vectors and facilitate vector control by predicting that spatially-targeted, proactive interventions would be more efficacious than current, reactive approaches.
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Molecular research and the control of Chagas disease vectors
Article
Full-text available
  • Sep 2005
  • AN ACAD BRAS CIENC
Chagas disease control initiatives are yielding promising results. Molecular research has helped successful programs by identifying and characterizing introduced vector populations and by defining intervention targets accurately. However, researchers and health officials are facing new challenges throughout Latin America. Native vectors persistently reinfest insecticide-treated households, and sylvatic triatomines maintain disease transmission in humid forest regions (including Amazonia) without colonizing human dwellings. In these scenarios, fine-scale vector studies are essential to define epidemiological risk patterns and clarify the involvement of little-known triatomine taxa in disease transmission. These eco-epidemiological investigations, as well as the planning and monitoring of control interventions, rely by necessity on accurate taxonomic judgments. The problems of cryptic speciation and phenotypic plasticity illustrate this need – and how molecular systematics can provide the fitting answers. Molecular data analyses also illuminate basic aspects of vector evolution and adaptive trends. Here we review the applications of molecular markers (concentrating on allozymes and DNA sequencing) to the study of triatomines. We analyze the suitability, strengths and weaknesses of the various techniques for taxonomic, systematic and evolutionary investigations at different levels (populations, species, and higher taxonomic categories).
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Arlequin (version 3.0): An integrated software package for population genetics data analysis
Article
Full-text available
Arlequin ver 3.0 is a software package integrating several basic and advanced methods for population genetics data analysis, like the computation of standard genetic diversity indices, the estimation of allele and haplotype frequencies, tests of departure from linkage equilibrium, departure from selective neutrality and demographic equilibrium, estimation or parameters from past population expansions, and thorough analyses of population subdivision under the AMOVA framework. Arlequin 3 introduces a completely new graphical interface written in C++, a more robust semantic analysis of input files, and two new methods: a Bayesian estimation of gametic phase from multi-locus genotypes, and an estimation of the parameters of an instantaneous spatial expansion from DNA sequence polymorphism. Arlequin can handle several data types like DNA sequences, microsatellite data, or standard multilocus genotypes. A Windows version of the software is freely available on http://cmpg.unibe.ch/software/arlequin3.
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The insect cytochrome oxidase I gene: evolutionary patterns and conserved primers for phylogenetic studies
Article
Full-text available
  • Aug 1996
Insect mitochondrial cytochrome oxidase I (COI) genes are used as a model to examine the within-gene heterogeneity of evolutionary rate and its implications for evolutionary analyses. The complete sequence (1537 bp) of the meadow grasshopper (Chorthippus parallelus) COI gene has been determined, and compared with eight other insect COI genes at both the DNA and amino acid sequence levels. This reveals that different regions evolve at different rates, and the patterns of sequence variability seems associated with functional constraints on the protein. The COOH-terminal was found to be significantly more variable than internal loops (I), external loops (E), transmembrane helices (M) or the NH2 terminal. The central region of COI (M5-M8) has lower levels of sequence variability, which is related to several important functional domains in this region. Highly conserved primers which amplify regions of different variabilities have been designed to cover the entire insect COI gene. These primers have been shown to amplify COI in a wide range of species, representing all the major insect groups; some even in an arachnid. Implications of the observed evolutionary pattern for phylogenetic analysis are discussed, with particular regard to the choice of regions of suitable variability for specific phylogenetic projects.
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MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment
Article
Full-text available
  • Jun 2004
With its theoretical basis firmly established in molecular evolutionary and population genetics, the comparative DNA and protein sequence analysis plays a central role in reconstructing the evolutionary histories of species and multigene families, estimating rates of molecular evolution, and inferring the nature and extent of selective forces shaping the evolution of genes and genomes. The scope of these investigations has now expanded greatly owing to the development of high-throughput sequencing techniques and novel statistical and computational methods. These methods require easy-to-use computer programs. One such effort has been to produce Molecular Evolutionary Genetics Analysis (MEGA) software, with its focus on facilitating the exploration and analysis of the DNA and protein sequence variation from an evolutionary perspective. Currently in its third major release, MEGA3 contains facilities for automatic and manual sequence alignment, web-based mining of databases, inference of the phylogenetic trees, estimation of evolutionary distances and testing evolutionary hypotheses. This paper provides an overview of the statistical methods, computational tools, and visual exploration modules for data input and the results obtainable in MEGA.
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PHYLOGENY AND EVOLUTION OF PARTHENOGENETIC WEEVILS OF THE ARAMIGUS TESSELLATUS SPECIES COMPLEX (COLEOPTERA: CURCULIONIDAE: NAUPACTINI): EVIDENCE FROM MITOCHONDRIAL DNA SEQUENCES
Article
  • Apr 1996
  • EVOLUTION
Molecular-phylogenetic studies of parthenogenetic animals have been a valuable recent addition to the literature on the evolutionary biology of sex. By illuminating the origins and ages of parthenogenetic lineages, such studies can help to define the temporal scale at which selection acts against parthenogenetic lineages, as well as provide an essential framework for further study. Although parthenogenetic weevils have played an important role in cytogenetic and protein-electrophoretic studies of parthenogenesis, they have not previously been subjects of DNA-based molecular-phylogenetic study. A mitochondrial DNA study of Aramigus tessellatus, a species complex of weevils native to South America, indentified 12 distinct (1-9% divergent) maternal lineages, of which 2 represent sexual populations, while at least 9 represent parthenogenetic lineages. These lineages partially correspond to lineages previously recognized by morphological differences. Phylogenetic analysis found 14 most parsimonious trees, according to which parthenogenesis appears to have arisen 3-7 times. There is a monophyletic group of lineages (the "brown clade"), having up to 4.5% sequence divergence within it, which may be primitively parthenogenetic and over 2 million years old.
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CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP
Article
  • Jul 1985
  • EVOLUTION
The recently-developed statistical method known as the "bootstrap" can be used to place confidence intervals on phylogenies. It involves resampling points from one's own data, with replacement, to create a series of bootstrap samples of the same size as the original data. Each of these is analyzed, and the variation among the resulting estimates taken to indicate the size of the error involved in making estimates from the original data. In the case of phylogenies, it is argued that the proper method of resampling is to keep all of the original species while sampling characters with replacement, under the assumption that the characters have been independently drawn by the systematist and have evolved independently. Majority-rule consensus trees can be used to construct a phylogeny showing all of the inferred monophyletic groups that occurred in a majority of the bootstrap samples. If a group shows up 95% of the time or more, the evidence for it is taken to be statistically significant. Existing computer programs can be used to analyze different bootstrap samples by using weights on the characters, the weight of a character being how many times it was drawn in bootstrap sampling. When all characters are perfectly compatible, as envisioned by Hennig, bootstrap sampling becomes unnecessary; the bootstrap method would show significant evidence for a group if it is defined by three or more characters.
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Spatio-temporal analysis of reinfestation by Triatoma infestans (hemiptera : reduviidae) following insecticide spraying in a rural community in northwestern Argentina
Article
  • Dec 2004
The spatio-temporal reinfestation patterns by Triatoma infestans following a blanket insecticide spraying in the rural community of Amama in northwestern Argentina were analyzed using a geographic information system, satellite imagery, and spatial statistics. Domestic and peridomestic reinfestation by triatomine bugs was monitored from 1993 to 1997. Triatoma infestans was detected at least once in 75% of 2,110 sites evaluated. The prevalence of sites positive at least once for T. infestans during the study period increased sharply from 1993-1995 (0.6-2.9%) to November 1997 (32%). The initial source of T. infestans was a pig corral in southern Amama one year post-spraying. Subsequent infestations were clustered around this initial focus at a distance of approximately 400 meters starting in 1995. In 1996, clustering was maximized in sites within the same or in neighboring compounds at distances of 25-175 meters. An effective control program on the community level will be based on the spraying of actual epicenters and sites within 450 meters of these epicenters to prevent the propagation of T. infestans.
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