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T. dimidiata

T. dimidiata is the most important Chagas vector in southern Mexico, Central America, and a secondary vector, after R. prolixus, in northern South America (Fig. 8.6). The diversity of this species across its geographic range in morphologic, behavioral, phenotypic, and genetic characteristics has resulted in its being split and merged many times into various species and subspecies (reviewed in Ref 38). Many variable attributes have significant implications for the epidemiological importance of particular populations (e.g., domestic or sylvan habitat, blood source preference). This diversity across a large geographic range and presence in multiple ecotopes make it quite challenging to control, and local approaches are needed for the different local conditions.

Cryptic species within T. dimidiata

Cross breeding studies66 combined with genetic data including nuclear, mitochondrial, and cytogenetic data27,38,67,68 identify the geographic range of cryptic species to include Yucatan, Mexico; Belize; Peten, Guatemala; and Yoro, Honduras. However, since the various studies were done on different individuals, it is not clear if there is one or more cryptic species.

The most comprehensive T. dimidiata phylogeny to date, combining both nuclear and mitochondrial DNA markers on the same individuals, shows there is likely at

Approximate current distribution of T. dimidiata

Figure 8.6 Approximate current distribution of T. dimidiata.

Source: Data from World Health Organization. Geographical distribution of arthropod-borne diseases and their principal vectors. WHO/VBC/89.967, Geneva; 1989.65 Artist: Linda Waller; Photographer: James Gathany (Centers for Disease Control and Prevention).

least two cryptic species and a large diverse clade, T. dimidiata s.s.69. This result indicates that population genetic studies conducted in areas with cryptic species must be interpreted with caution. Specimens from areas without reported cryptic species will be referred to as T. dimidiata s.s. below.

Unlike the mostly domestic nature of T. infestans, T. dimidiata occupies domestic, peridomestic, and sylvatic ecotopes over its geographic range. Interestingly, the distribution among ecotopes is quite different among geographic populations. T. dimidiata is nearly exclusively domestic and peridomestic over most of its range, from southern Mexico (except the Yucatan peninsula), southern Guatemala to Costa Rica and Ecuador, as well as the central Andean region of Colombia. However, it is largely sylvatic with occasional or seasonal entry into houses in northern Guatemala, the Yucatan peninsula in Mexico, and in the Caribbean plains and Sierra Nevada de Santa Marta mountains in Colombia. , , , The distinct habitats occupied, the degree of migration among habitats, as well as the underlying demographic history have been implicated in shaping the current patterns of genetic diversity for T. dimidiata across its geographic range.

Genetic variation and structure in T. dimidiata populations

In spite of the distribution of T. dimidiata populations among different ecotopes, and with limited studies to date, a consistent pattern emerges of T. dimidiata as a highly mobile species migrating between sylvan and domestic/peridomestic ecotopes13 or simply between domestic ecotopes (among houses and villages) in regions where it is largely domestic and there is little remnant forest.14 T. dimidiata shows high genetic diversity, perhaps as a result of different selective pressures in the different ecotopes and genetic mixing between populations. Populations tend to show limited genetic structure at small distances (the evidence for high migration), and greater subdivision over larger geographic areas. In Central America, across large geographic distances there is support for the Isolation by Distance model of population subdivision42; whereas demographic history appears to play a larger role than Isolation by Distance in Colombia (described later).

Studies using both nuclear and mitochondrial DNA sequence show high diversity across large geographic regions in Central America. In Costa Rica, T. dimidiata s.s. populations from seven localities including both domestic/peridomestic and sylvan ecotopes were surprisingly monomorphic for the nuclear ITS-2 gene but genetically differentiated based on mitochondrial cyt b sequences26 (Table 8.2) (Hd = 0.901). The ~ 200 km between the two regions which shared only one of 15 haplotypes, likely contributes to the genetic diversity.

Although with too few samples for statistical analysis, high genetic variation was also observed in mitochondrial ND4 and cyt b genes among 15 T. dimidiata sampled across central and southern Guatemala (Hd = 0.924).71

In Colombia, three studies comparing T. dimidiata from domestic/peridomestic and sylvan ecotopes across three ecogeographic regions (northern Caribbean plains, Sierra Nevada de Santa Marta mountain, and central Inter-Andean valleys) using mitochondrial and microsatellite markers show high genetic diversity and population subdivision. The first study, with limited sampling and using the mitochondrial marker ND4, shows high haplotype diversity (Hd = 0.863) and significant population subdivision (Ф = 0.761), that weakly correlates with Isolation by Distance.28 The second study, with a broader sampling and using mitochondrial coI also shows high genetic diversity (Hd = 0.985) and strong genetic structure (FST = 0.225),15 results supported by microsatellite markers in the same study. Haplotypes clustered geographically with evidence of rare gene flow between the mountain and plains (the two nearest regions), and some subdivision within Caribbean plains. Again, results weakly supported Isolation by Distance. The third study with extensive sampling and again using the mitochondrial gene ND4 showed high genetic diversity and genetic differentiation within and among regions (overall Hd = 0.991) and strong structure (FST = 0.482), which could not be explained by Isolation by Distance.29 With this larger sampling population, subdivision appears to be due to recent (> ~4.5 mya) population expansion after the joining of the continents with the formation of the Isthmus of Panama and differentiation influenced by isolation and drift of the populations with the upwelling of the Andes. Demographic history may be more important in Colombia rather than Isolation by Distance, better explaining the population structure.

In the Yucatan Peninsula, Mexico, microsatellites revealed weak population structure where T. dimidiata enters houses seasonally but does not establish domestic colonies, migrating between sylvan and domestic/peridomestic ecotopes. Analysis of only three microsatellites in and around 14 villages indicated high migration among nearby houses (FST = 0.037), more distant houses (FST = 0.055, <250 km), and between forest and houses (FST = 0.01—0.03, <280 km).13 Longer distance migration could be due to passive transport. High migration was also indicated by 10—22% of domestic insects being more similar to those from peridomestic or sylvatic habitats. However, the recently described cryptic species occurs in this area (along with putative hybrids),36 so these results must be interpreted with caution.

In Guatemala, microsatellite studies among domestic populations from six nearby villages (<27 km) showed small but significant differentiation (FST = 0.05) among populations; shared genetic clusters indicated some limited migration.14 Although apparently T. dimidiata s.s. in Central America is moving less than in Yucatan, Mexico, the finding that in nearly all houses insects were half-sibs to completely unrelated suggests frequent migration is occurring, in this case among houses and villages rather than between ecotopes.

Implications for control and future studies for T. dimidiata

From the data to date, T. dimidiata s.l. appears to have generally higher diversity and movement than T. infestans. In localities where it is exclusively domestic and peridomestic, T. dimidiata moves readily among houses within villages and among nearby villages. Where sylvatic populations exist, insects transiently enter homes. Evidence suggests long-distance, passive dispersal in human belongings or agricultural products. Broad geographic sampling shows Isolation by Distance occurs in Central America but not in Colombia.

Because of the extensive peridomestic and sylvatic populations and high migration, simply spraying insecticide in houses is unlikely to be effective for vector control. Ecohealth strategies, including house improvements, community participation, and control strategies designed for local situations will be more effective and sustainable.72 Areas in need of further research include population genetics studies to determine the geographic range of differentiated subpopulations and their epidemiological importance. In addition, it will be important to determine the geographic, environmental, and anthropogenic factors keeping subpopulations apart, as well as the effects of Ecohealth interventions compared to traditional spraying on the population genetics of T. dimidiata.

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