Entomological parameters and population structure at a microgeographic scale of the main Colombian malaria vectors Anopheles albimanus and Anopheles nuneztovari

PLOS ONE RESEARCH ARTICLE Entomological parameters and population structure at a microgeographic scale of the main Colombian malaria vectors Anopheles albimanus and Anopheles nuneztovari Mariano Altamiranda-Saavedra1,2‡, Nelson Naranjo-Dı́az1,2‡, Jan E. Conn ID3,4, Margarita M. Correa ID1* a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 1 Grupo de Microbiologı́a Molecular, Escuela de Microbiologı́a, Universidad de Antioquia, Medellı́n, Colombia, 2 Grupo de Investigación Bioforense, Tecnológico de Antioquia, Medellı́n, Colombia, 3 New York State Department of Health, Wadsworth Center, Albany, NY, United States of America, 4 Department of Biomedical Sciences, School of Public Health, State University of New York-Albany, Albany, NY, United States of America ‡ MAS and NND are share first authorship on this work. * OPEN ACCESS Citation: Altamiranda-Saavedra M, Naranjo-Dı́az N, Conn JE, Correa MM (2023) Entomological parameters and population structure at a microgeographic scale of the main Colombian malaria vectors Anopheles albimanus and Anopheles nuneztovari. PLoS ONE 18(1): e0280066. https://doi.org/10.1371/journal. pone.0280066 Editor: Luzia H. Carvalho, Fundação Oswaldo Cruz Centro de Pesquisas René Rachou: Fundacao Oswaldo Cruz Instituto Rene Rachou, BRAZIL Received: July 22, 2022 Accepted: December 20, 2022 Published: January 6, 2023 Copyright: This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: This research received funding from Escuela de Microbiologı́a, Universidad de Antioquia (https://www.udea.edu.co), project code No. 202141851 to MMC and was partly supported by The US National Institutes of Health (https://www.nih. Abstract Population subdivision among several neotropical malaria vectors has been widely evaluated; however, few studies have analyzed population variation at a microgeographic scale, wherein local environmental variables may lead to population differentiation. The aim of the present study was to evaluate the genetic and geometric morphometric structure of Anopheles nuneztovari and Anopheles albimanus in endemic localities of northwestern Colombia. Genetic and phenetic structures were evaluated using microsatellites markers and wing geometric morphometrics, respectively. In addition, entomological indices of importance in transmission were calculated. Results showed that the main biting peaks of Anopheles nuneztovari were between 20:00 and 22:00, whereas Anopheles albimanus exhibited more variation in biting times among localities. Infection in An. nuneztovari by Plasmodium spp. (IR: 4.35%) and the annual entomological inoculation rate (30.31), indicated high vector exposure and local transmission risk. We did not detect Plasmodium-infected An. albimanus in this study. In general, low genetic and phenetic subdivision among the populations of both vectors was detected using a combination of phenotypic, genetic and environmental data. The results indicated high regional gene flow, although local environmental characteristics may be influencing the wing conformation differentiation and behavioral variation observed in An. albimanus. Furthermore, the population subdivision detected by microsatellite markers for both species by Bayesian genetic analysis provides a more accurate picture of the current genetic structure in comparison to previous studies. Finally, the biting behavior variation observed for both vectors among localities suggests the need for continuous malaria vector surveys covering the endemic region to implement the most effective integrated local control interventions. PLOS ONE | https://doi.org/10.1371/journal.pone.0280066 January 6, 2023 1 / 19 PLOS ONE gov), R01 grant 2R01 AI110112 to JEC. Specimens analyzed are part of collections performed under project funded by Colciencias (Now Minciencias: Ministerio de Ciencia Tecnologı́a e Innovación) code No. 596-2013, to MMC. The funders have played no role in the research. There was no additional external funding received for this study. Competing interests: The authors have declared that no competing interests exist. Population structure of malaria vectors at a microgeographic scale Introduction Malaria remains one of the most important public health problems worldwide. The Plasmodium parasites that cause the disease are transmitted to humans by the female mosquitoes of approximately 40 species of Anopheles [1]. Colombia is third in the number of malaria cases in the Americas [2], and the number of cases/year in the past five years has fluctuated between 50,000–80,000 [3–7]. Currently, the most malaria endemic regions are the Pacific (PAC) in western Colombia (49.2%), and the Urabá-Bajo Cauca-Alto Sinú (UCS), in the northwest (18.7%) [3]. During the study period (2013–2014), the number of malaria cases registered in UCS were 22,889 (2013) and 8,620 (2014), corresponding to 43.84% and 20.97% of the cases in the country, respectively [8, 9]. The main malaria vectors in Colombia are Anopheles darlingi, Anopheles nuneztovari and Anopheles albimanus [10, 11]. Vector control is one of the main strategies to decrease malaria incidence [1]; thus, knowledge of vector biology remains essential to reduce malaria transmission. It is known that anthropogenic environmental alterations and insecticide selection pressures affect vector population dynamics, because these factors may increase the abundance of anthropogenic Anopheles species and the appearance of insecticide resistant species, which affect malaria risk parameters [12–14]. Hence, genetic population structure and entomological parameters should be regularly monitored to evaluate changes in transmission risk to implement Integrated Vector Management programs [15]; such information will allow, for example, the identification of season(s) when vector control interventions should be intensified. Population structure studies of the neotropical malaria vectors An. nuneztovari and An. albimanus have identified population subdivision across their distributions [16, 17]. Regarding An. nuneztovari, several lineages were identified among South American populations [18], and a new species of the Nuneztovari Complex, lineage III, has been identified east of the Amazon region [19]. In Colombia, genetic differentiation and population subdivision was detected between An. nuneztovari populations from the west-northwest and the east-northeast, attributed to physical barriers, geographic distance and ecological variation on both sides of the Andes [20]. However, a study using COI and the white gene found high gene flow and the existence of a single taxon in An. nuneztovari from UCS, northwest Colombia [ (...truncated)