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Gene Flow Among Anopheles Albimanus Populations in Central America, South America, and the Caribbean Assessed by Microsatellites and Mitochondrial Dna

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Gene Flow Among Anopheles Albimanus Populations in Central America, South America, and the Caribbean Assessed by Microsatellites and Mitochondrial Dna Am. J. Trop. Med. Hyg., 71(3), 2004, pp. 350–359 Copyright © 2004 by The American Society of Tropical Medicine and Hygiene GENE FLOW AMONG ANOPHELES ALBIMANUS POPULATIONS IN CENTRAL AMERICA, SOUTH AMERICA, AND THE CARIBBEAN ASSESSED BY MICROSATELLITES AND MITOCHONDRIAL DNA ALVARO MOLINA-CRUZ, ANA MARI´AP.DEME´ RIDA, KATHERINE MILLS, FERNANDO RODRI´GUEZ, CAROLINA SCHOUA, MARI´A MARTA YURRITA, EDUVIGES MOLINA, MARGARITA PALMIERI, AND WILLIAM C. BLACK IV Universidad del Valle de Guatemala, Guatemala City, Guatemala; Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, Colorado Abstract. Gene flow was examined among Anopheles albimanus populations from Cuba, Mexico, Guatemala, El Salvador, Nicaragua, Costa Rica, Panama, Colombia, and Venezuela by examining variation at four microsatellite (MS) loci and a mitochondrial DNA (mtDNA) marker. There was little variation among Central American populations and weak isolation by distance was only observed with the MS loci. There was moderate to large variation between Central and South American populations, suggesting a barrier to gene flow between Central and South America. However, Panamanian and Pacific Costa Rican populations differed with respect to western Central America, suggesting that there may be another barrier within Central America. There was small to moderate variation among Caribbean and conti- nental populations. Phylogenetic and diversity analyses of mtDNA indicate that more ancestral and diverse haplotypes were present in the Caribbean population, suggesting that current continental An. albimanus populations may have originated from the Caribbean. INTRODUCTION larger An. albimanus collections from throughout Central and South America and the Caribbean. Anopheles albimanus Wied. is the primary coastal vector of malaria from southern Mexico to northern Peru, and in the MATERIALS AND METHODS Greater Antilles.1 The species is found mainly at an altitude < 100 meters in a wide range of larval habitats that vary from Mosquito collections and extraction of DNA. The loca- hoof prints to lakes and brackish water.2 Anopheles albi- tions, collectors, and sample sizes of An. albimanus collec- manus populations vary considerably in their vector compe- tions in Central and South America and the Caribbean are tence for human malarias, their biting behavior, and host listed in Table 1, and the geographic locations of all sampling preference,2 even though the species is cytologically3 and sites are shown in Figure 1. Some of the collections from morphologically4 constant throughout its range. Knowledge Guatemala and one from Costa Rica were used in a previous of population structure can help make predictions of migra- study.8 Mosquitoes were collected in cattle corrals and kept tion among vector populations, give insights into the epide- alive for 24 hours in cardboard cartons with sugared water. miology and transmission of malaria, and help in the design of Afterwards, they were frozen and placed in 70% ethanol more effective vector control,5,6 including the possible release awaiting extraction of DNA.8 The DNA samples of An. bel- of genetically modified vectors.7 lator and An. cruzi individuals collected on the island of Trin- In a previous study,8 we examined the distribution of mi- idad and in Sao Paulo State, Brazil, respectively, were kindly tochondrial DNA haplotypes among An. albimanus collec- provided by Dr. Richard Wilkerson (Museum Support Cen- tions in Guatemala, to test for gene flow barriers using a ter, Smithsonian Institution, Suitland, MD). 390-basepair region of the mitochondrial NADH dehydroge- Microsatellite loci isolation, amplification, and identifica- nase subunit 5 (ND5) gene. Phylogenetic analysis among the tion. Anopheles albimanus genomic DNA was digested with 15 most common haplotypes did not detect clades associated Mbo I and subjected to electrophoresis on a 1.5% agarose gel. with geographic regions. Collections from different regions of DNA between 300 and 1,000 basepairs was separated and Guatemala were genetically similar, as were collections from purified from the gel. Digested DNA was ligated to Bam the same locations across three seasons. These results sug- HI-digested pBluescript plasmid (Stratagene, La Jolla, CA). gested that an earlier study of the An. albimanus ribosomal Recombinant colonies containing MS loci were identified by 9 32 DNA intergenic spacer (IGS) had overestimated genetic dif- hybridization with P-labeled (AG)20 and (AC)20 probes. ferences between Atlantic and Pacific populations, possibly Selected MS clones were sequenced and polymerase chain due to concerted evolution.8 Evidence from independent reaction (PCR) primers were designed and tested with An. nuclear markers was therefore required to support the results albimanus DNA from different geographic regions. The MS obtained with the ND5 marker. The earlier ND5 study8 also loci selected contained mostly AG repeats except for MS 1-90 suggested barriers to gene flow in Costa Rica and Panama and 6-41, which were composite microsatellites containing with respect to western Central America, and that ND5 hap- both AC and AG repeats. lotype frequencies in South America differed significantly Microsatellite locus 1-90 was amplified in single mosquitoes with respect to Central America. using primers 1-90+ (5Ј-GCA TAA ATA ATA GCC AA The present study expands on our previous findings on the CA-3Ј) and 1-90- (5Ј-GTC ACA CTT CCG ACT ACA AA- population structure and phylogenetic relationships among 3Ј). Microsatellite locus 2-14 was amplified with primers 2-14+ An. albimanus populations of Central and South America. In (5Ј-GCC CTT GCC AAG ATA AAA TGG AAA-3Ј) and this study, four microsatellite (MS) markers have been used, 2-14- (5Ј-TCA AAT AAT CCT AAA ACA CCG TCC-3Ј). in addition to the ND5 mitochondrial marker, to characterize Microsatellite locus 2-25 was amplified using primers 2-25+ 350 GENE FLOW AMONG AN. ALBIMANUS POPULATIONS 351 TABLE 1 Locations, collectors, regions, dates, and samples sizes of Anopheles albimanus collections* Region Country (collector) Sub-region ND5 MS Collection site date (n for ND5, n for MS) n n Caribbean 146 170 Cuba 146 170 1) La Habana (I. Garcia) 5/19/99 146 170 Central America 1,575 1,110 Mexico, Chiapas 143 150 2) Zapata 12/1/98 47 50 3) Cossalapa 12/1/98 48 50 4) N. Independencia 12/19/98 48 50 Guatemala (N. Padilla, C. C. de Roslaes, P. Peralta, J. Garcia) 923 422 Northern Guatemala 298 115 5) Champona 3/6/95 (12, 0), 7/6/95 (32, 0), 9/5/95 (43, 0), 3/11/96 (0, 37) 8737 6) Nahua 3/9/95 (9, 0), 7/3/95 (43, 0), 9/6/95 (43, 0) 81 24 7) S. Luis Peten PE 7/10/95 (43, 0), 3/12/01 (0, 31) 43 31 8) S. Luis Peten BV 7/10/95 (43, 0), 9/4/95 (44, 0), 3/12/01 (0, 23) 87 23 Southern Guatemala 443 211 9) Cuto 2/6/95 (42, 0), 6/5/95 (26, 0), 4/5/95 (89, 0), 3/27/96 (0, 48) 147 48 10) Lauro 6/7/95 (4, 0), 4/4/95 (19, 0), 2/9/95 (31, 0), 3/27/96 (0, 14), 6/7/96 (0, 13) 54 27 11) Mango 3/15/95 (22, 0), 2/28/96 (33, 32), 3/7/96 (37, 0) 92 32 12) Ruperto 2/8/95 (16, 0), 6/7/95 (16, 0), 4/3/95 (9, 0), 10/4/95 (0, 48), 3/27/96 (0, 16) 41 64 13) Tallado 6/5/95 (12, 0), 2/7/95 (40, 40), 8/2/95 (38, 0), 6/6/95 (9, 0) 99 40 Eastern Guatemala 182 96 14) El Motor 3/20/96 45 48 15) Puente Blanco 7/11/95 (46, 0), 2/21/96 (46, 48), 9/11/95 (45, 0) 137 48 El Salvador (H. Francia) 125 149 16) San Alfredo 10/21/98 42 50 17) San Diego 10/21/98 39 50 18) Sta Lucia 10/21/98 44 39 Nicaragua (E. Lugo) 136 150 19) Corral 1 9/24/98 46 50 20) Corral 2 9/24/98 47 50 21) Corral 3 9/30/98 43 50 Costa Rica (T. Solano) 159 120 Atlantic Ocean Coast 95 120 22) Bananito 4/13/99 46 60 23) Batan 4/13/99 49 60 Pacific Ocean Coast 64 ND 24) Puntarenas 95 64 ND Panama (A. Ying) 89 119 25) Corral 1a 2/23/99 49 59 26) Corral 1b 2/23/99 40 60 South America 144 131 Colombia 47 49 27) El Carmen (V P. Howley) 91 47 49 Venezuela (Y. Rangel) 97 82 28) Corral Magdalena 8/99 30 50 29) Corral Puertas Negra 8/99 67 32 Total 1,865 1,411 * Samples sizes are indicated in parentheses when multiple collections were taken at a site. .not determined ס microsatellite; ND ס NADH dehydrogenase subunit 5, MS ס ND5 (5Ј-GGT TTC CAG CCT CCA TTC TC-3Ј) and 2-25- (5Ј- Mitochondrial gene amplification and haplotype identifica- CCT TAC TGT GCT GGA ACA CG-3Ј). Microsatellite lo- tion. The ND5 gene was amplified in individual mosquitoes cus 6-41 was amplified using primers 6-41+ (5Ј-CGG CAT using primers ND5P1 (5Ј-TWG CSC CTA ATC CKG CTA CCA TCC TTT CTC TG-3Ј) and 6-41- (5Ј-GAC CTC GCG TA-3Ј) and ND5M2 (5Ј-YTW GGA TGA GAT GGS TTA ,CorG ס purine, S ס pyrimidine, R ס CCT TGT CAT AA-3Ј). GG-3Ј), where Y -A or T. The amplified regions corre סGorT,andW ס Amplified MS alleles were size fractionated by electropho- K resis on denaturing DNA sequencing gels and visualized by spond with nucleotides 7,282-7,671 in An. quadrimaculatus silver staining.10 On each gel, the reciprocal of the length of (GenBank #L04272) and nucleotides 7,169-7,558 in An.
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