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Background: Aedes aegypti is the primary vector of the four serotypes of dengue virus (DENV1-4), Chikungunya and yellow fever virus to humans. Previous population genetic studies have revealed a particular genetic structure among the vector populations in the Americas that suggests differences in the ability to transmit DENV. In Colombia, despite its high epidemiologic importance, the genetic population structure and the phylogeographic depiction of Ae. aegypti, as well as its relationship with the epidemiologic landscapes in cities with heterogeneous incidence levels, remains unknown. We conducted a spatiotemporal analysis with the aim of determining the genetic structure and phylogeography of Colombian populations of Ae. aegypti among cities with different eco-epidemiologic characteristics with regard to DENV. Methods/Findings: Mitochondrial cytochrome oxidase C subunit 1 (COI) - NADH dehydrogenase subunit 4 (ND4) genes were sequenced and analyzed from 341 adult mosquitoes collected during 2012 and 2013 in the Colombian cities of Bello, Riohacha and Villavicencio, which exhibit low, medium and high levels of incidence of DENV, respectively. The results demonstrated a low genetic differentiation over time and a high genetic structure between the cities due to changes in the frequency of two highly supported genetic groups. The phylogeographic analyses indicated that one group (associated with West African populations) was found in all the cities throughout the sampling while the second group (associated with East African populations) was found in all the samples from Bello and in only one sampling from Riohacha. Environmental factors such as the use of chemical insecticides showed a significant correlation with decreasing genetic diversity, indicating that environmental factors affect the population structure of Ae. aegypti across time and space in these cities. Conclusions: Our results suggest that two Ae. aegypti lineages are present in Colombia; one that is widespread and related to a West African conspecific, and a second that may have been recently introduced and is related to an East African conspecific. The first lineage can be found in cities showing a high incidence of dengue fever and the use of chemical insecticides, whereas the second is present in cities showing a low incidence of dengue fever where the use of chemical insecticides is not constant. This study helps to improve our knowledge of the population structure of Ae. aegypti involved in the diversity of dengue fever epidemiology in Colombia. Author Summary: Knowledge on the population structure of Aedes aegypti, the main vector of the dengue virus (DENV), is essential to improving dengue fever prevention strategies in endemic countries. In Colombia, despite the epidemiological relevance of dengue fever, the genetic population structure and phylogeography of the vector Ae. aegypti is little known. In this study, we evaluated the spatio-temporal structure and phylogeography of Colombian Ae. aegypti populations from cities showing different eco-epidemiologic attributes related to dengue fever. Our results indicated that Colombian Ae. aegypti populations harbor two mitochondrial lineages related to West and East African ancestors. The lineage related to West African populations is the most frequent and widely distributed in Colombia, and it was found in cities with a high incidence of the dengue fever. A second lineage related to East African populations, which may have been recently introduced in some regions, was found in cities showing a low incidence of dengue. These findings suggest complex population dynamic is involved in dengue fever epidemiology in Colombia, and indicate further studies about biological attributes of the Ae. aegypti lineages should be performed. [ABSTRACT FROM AUTHOR]