A New Cytotype of Anopheles Nuneztovari from Western Venezuela and Colombia

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A New Cytotype of Anopheles Nuneztovari from Western Venezuela and Colombia Journal of the American Mosquito Contol Association,9(3\:294-301, 1993 A NEW CYTOTYPE OF ANOPHELES NUNEZTOVARI FROM WESTERN VENEZUELA AND COLOMBIA JAN CONN,'2 YADIRA RANGEL PUERTAS,,tND JACK A. SEAWRIGHT3 ABSTRACT. Cytogeneticanalysis of the larval polytenechromosomes of Anophelesnuneztovari from 5 collection sites in T6chira and Zulia statesnorthwest of the Andean Cordillera in westem Venezuela and from 2 sitesin the Department of Valle, westernColombia, revealedwhat appearsto be a distinctive cytotype informally designatedas An. nuneztovariC.lts chromosomesare homosequentialwith those of An. nuneztovariB from westernVenezuela southeast ofthe Cordillera but differ in the presenceofa well- defined chromocenter and unique inversion polymorphisms. The large complex inversion in western Venezuela, 2Lb, is present at a frequency of 0.263 and deviates significantly from Hardy-Weinbery equilibrium in 3 of the 5 sites.Two smaller inversions (2Ir and 2Id) that are included in 2Lb arepresent in the Colombian samplesat a frequency of 0.300. INTRODUCTION Anophelesnuneztovari has been incriminated as the main vector of the malaria parusite,Plas- The distribution of the malaria vector Anoph- modium vlvax (Grassi and Feletti), in northern eles nuneztovari Gabald,6n includes an extensive Colombia and westernVenezuela (Gabald6n and portion of northern South America (Fig. 1) as Guerrero 1959,Gabald6n et al. 1963).More re- well as eastern Panama (Faran 1980). Early be- cently, results of monoclonal antibody havioral and ecological observations (Elliott surveys ofCS proteins and/or salivary gland 1972) as well as cytological differences (Kitz- dissections for sporozoiteshave implicated An. nuneztovari miller et al. 1973) suggested that An. nuneztovari in the transmission of P. vivax in Par6 State, consisted of 2 geographically distinctive popu- Brasil (de Armda et al. 1986),eastern Peru (Hayes lations, one a nonvector in the Amazonian drain- et al. 1987) and Amap6 Brasil (Tadei age basin and the other a vector in western Ven- State, et al. I 99 I as well in ezuela and northern Colombia. These populations ), as the transmission of Plas- modiumfalciparumin Amap6 State(Tadei et al. have been designated informally as A (Amazo- 199l). These findings nian) and B (Colombian/Venezuelan) (Conn confound the earlier, sim- pler hypothesis of vector and nonvector 1990) and can be distinguished cytologically by status of An. nuneztovaribased,primarily on geograph- a fixed inversion in the XR arm (Kitzmiller et ical distribution (Kitzmiller et al. 1973). al. 1973). Unfortunately, no voucher specimens In this report, we present evidence for a dis- from the collection sites of Kitzmiller et al. (1973) tinctive cytotype, C, of An. nuneztovari from were saved to determine whether concomitant western Colombia and Venezuelanorthwest morphological differentiation existed. The re- of the Andean Cordillera, and we document the sults of an electrophoretic study (Steiner et al. existence of deviation from Hardy-Weinberg 1980) comparing samples from western Vene- equilibrium for the complex inversion 2Lb in zuela with Suriname showed allele frequency dif- Venezuela. ferences at the Est-5 locus that might be consid- ered diagnostic. The authors suggested, however, that additional sites and larger samples should MATERIALS AND METHODS be analyzed. Within Venezuela a comparative In Venezuela, larvae and adult females (the study of male genitalia of An. nuneztovari from latter for progeny rearings) were collected at 5 2 sites, one to the north and the other to the sites:Caffo Macho (8'22'0'N, 7221'0"W), Gua- south of the Andean Cordillera, suggested that ramito (8"13'48'N,72"19'59'W) and Moravia these represent 2 distinct populations (Avila Nu- (8"11'45'N, 72"21'14'W) in T6chira State;and fiez 1989a). Casigua(8'50'43'N, 72o30'10'W)and Rio So- cuav6(8'54'0'N, 72"38'0'W)in Zulia State(Figs. rPresent addressand address for reprint requests: 2 and 3). This area is just northwest of the An- % USDA/ARS, Medical and Veterinary Entomology dean Cordillera and southwest of Lake Mara- ResearchI-aboratory, P. O. Box 14565, Gainesville, caibo. The averagerainfall in the Maracaibo Ba- FL32604. sin variesfrom I,800 to 3,800mm annually,and 2 Instituto de Zoologia Tropical, Universidad Cen- the averagetemperature is 27"C. The mean al- tral de Venezuela, Caracas, Venezuela. 3 titude is 90 m above sealevel (Ewel et al. 1976). USDA/ARS, Medical and Veterinary Entomology The Colombian collection sites of Sitronela and Research Laboratory, Gainesville, FL 32604. a Avila Nufrez, J. L. 1989. Estudio bionomico de dos poblacionesde Anophelesnufteztovari Gabald6n, en el Occidente de Venezuela. Lic. Thesis. Univ. de 1940 (Diptera: Culicidae) separadas geograficamente los Andes. M6rida. Venezuela. 294 SBsrBlaseR1993 Anopnztz s wuNz zrovARI Cvrorvpr Details of larval rearing, salivary gland dis- section and polytene chromosome slide prepa- ration can be found in Conn (1990). From the venezuelan sites, chromosomes of 177 larvae were examined. Of these, 59 larvae were field collectedand l18 were F, progeny(l-2 larvae per female fro m a total of 72 mothers).The large, complex inversion polymorphism initially de- scribedby Kitzmilleret al. (1973)in the 2L chro- mosome arm has been named 2Lb following the convention ofColuzzi et al- (1973\. The break- points of the new inversion polymorphisms de- scribed here are based on the standard An. nu- neztovari chromosome map (Kitzmiller et al. 1973)and on the photomapofConn (1990).In the Department of Valle, Colombia, both larvae (n : 5) and Fr progeny (n : 8) from 5 adult females were analyzed from Zabaletas,and Ft progeny (n: 2) from one adult female from Si- tronela. Link-reared voucher specimens have depositedat the National Museum of Nat- l. The presumed distribution of the 3 cyto- been Fig. Washing- types(A, B and C) ofthe Anophelesnuneztovari species ural History, Smithsonian Institution, complex. ton, DC. Zabaletas are located at sea level near Buena- RESULTS ventura in the Cauca Valley (Fig. a). This valley is part ofthe marshy coastal lowland with a mean All larvae analyzed (Table l) had identical temperature of 27"C and an average annual rain- polytene chromosome banding pattems for all fall of 7,400 mm (Box 1990). chromosomes. The chromosomal banding pat- VENEZUELA Elevqtion lmeid I = ovet 975 ffi=500-9zs B = 200'500 I = Under200 Fig.2. Venezuela.The rectangleis the study area that is enlargedin Fig, 3. JounNal or rrrE ArusRlclN Moseutro Coxrrol Assocrlrror Vor-. 9, No. 3 o CASIGUA (0.l9tll rlA FRIA I o GUARAMITO (0.2651 o MORAVTA(0.0831 \ ffi oxm60 Fig. 3. The study area in westernVenezuela. The 5 collection sitesare Rio Socuav6,Casigua, Cafro Macho, Guaramito and Moravia. The frequencyof the inverted constituent (b) in the complex inversion 2Lb is found in brackets after each site. cotoMBlA Elevotion lmeled- = Ovet 2000 Buenoventuro | E = 975'2@0 & = 500'9zs I = Under500 Fig. 4. Colombia. Buenaventura is the nearest town to the collection sites of Sitronela and Zabaletas. SePTpr{spn1993 ANoPHE LE s vuugzrovtat CvtoTvpr 297 tern of An. nuneztovari C is also identical (i.e., Table l. Collections of An. nuneztovari C homosequential) to that of An. nuneztovari B from Venezuelaand Colombia used for from Barinas, Venezuela(Kitzmiller et al. 1973, cytogeneticanalysis. Conn 1990).However, one striking differenceis Collection Number the presenceof a marked chromocenter in each Location datet analyzed polytenecell of theAn. nuneztovariC mosquitoes (Fig. 5). l. Larval collections Severalpreviously unreported inversion poly- Venezuela morphisms were observed.Inversion 2Ra (l0A/ Caflo Macho July 18, 1989 2 B-l2AlB) was encountered in one larva from Nov. 8, 1989 4 Casigua. A single larva from Guaramito dis- June6, 1990 29 played inversion 3Ra (3lB/C-348). Inversion Guaramiro July 19, 1989 6 3Rb (28AlB-338) was observedin one larva from Casigua June 7, 1990 l8 Cafio Macho. A very small inversion loop in- volving 2 sets of double bands in the 3L arm Colombia "knot" 1992 s (3Lb, 38A/B-38C), was seenas a small Zabaletas Apm25, and found in 2 larvae from Cafio Macho. Asyn- 2. F, progeny from adult female collections apsis for the band in section l5,A',just proximal Venezuela to the sectionlimit l4l15 in the 2R arm (Fig. 5), Caffo Macho July 17, 1989 8 was detectedin 3 larvae from Casigua,in 4 from Nov. 7. 1989 9 Cafio Macho and in 2 from Guaramito. June5, 1990 4 The complex inversion (2Lb) involving much Guaramito Aug. 19, 1989 9 of the 2L arm was first described by lGtzmiller Nov. 8, 1989 19 et al. (1973, Fig. 8) basedon the analysisof 4 Moravia June6, 1990 l8 larvae collected from Casigua.This same inver- Rio Socuav6 July 8, l99l 14 sion was found from all 5 collection sitesin Ven- July 9, l99l 9 ezuela in the present study. A test for homoge- July 10, l99l 12 neity of genotype frequencies between the 5 Sept.22,1992 16 localities showed no significant differences for 2Lb (x2 -- 5-9O,4 df, P < 0.30). For the most Colombia 2 part we agreewith Kitzmiller et al. ( I 973) on the Sitronela Apil24,1992 designation of the major breakpoints (from the 7-,abaletas Apil26,1992 8 centromereto the limit of 22/23; Fig. 6), but the Total 192 larger synaptic region within this complex in- ' Datefor Fr progenyis thedate adults were caught. versionappears to extend from 19/20 to 2lA/B rather than regions2lB,2lC and 20A. We also determined that the included region from 16,4 had 2 inversions, 2I-c and 2l-d (Fig. 6), that ap- to l8C actually appearsto extend farther, from pear to be included within the complex 2Lb in- l6,4.to lgB/C. We agreethat the small inversion version from Venezuela. Inversion 2k com- 2La(15/16to l64lB) inAn. nuneztovariB(Kitz- mencesat the centromere(breakpoint I 5/ I 6) and miller et al- 1973,Conn 1990)is involved in the endsat l8B/C.
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