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Published in: Malaria Journal 1/2009

Open Access 01-12-2009 | Research

Assessing the molecular divergence between Anopheles (Kerteszia) cruzii populations from Brazil using the timeless gene: further evidence of a species complex

Authors: Luísa DP Rona, Carlos J Carvalho-Pinto, Carla Gentile, Edmundo C Grisard, Alexandre A Peixoto

Published in: Malaria Journal | Issue 1/2009

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Abstract

Background

Anopheles (Kerteszia) cruzii was the most important vector of human malaria in southern Brazil between 1930–1960. Nowadays it is still considered an important Plasmodium spp. vector in southern and south-eastern Brazil, incriminated for oligosymptomatic malaria. Previous studies based on the analysis of X chromosome banding patterns and inversion frequencies in An. cruzii populations from these areas have suggested the occurrence of three sibling species. In contrast, two genetically distinct groups among An. cruzii populations from south/south-east and north-east Brazil have been revealed by isoenzyme analysis. Therefore, An. cruzii remains unclear.

Methods

In this study, a partial sequence of the timeless gene (~400 bp), a locus involved in the control of circadian rhythms, was used as a molecular marker to assess the genetic differentiation between An. cruzii populations from six geographically distinct areas of Brazil.

Results

The timeless gene revealed that An. cruzii from Itaparica Island, Bahia State (north-east Brazil), constitutes a highly differentiated group compared with the other five populations from south and south-east Brazil. In addition, significant genetic differences were also observed among some of the latter populations.

Conclusion

Analysis of the genetic differentiation in the timeless gene among An. cruzii populations from different areas of Brazil indicated that this malaria vector is a complex of at least two cryptic species. The data also suggest that further work might support the occurrence of other siblings within this complex in Brazil.
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Literature
1.
go back to reference Pittendrigh CS: The ectopic specialization of Anopheles homunculus, and its relation to competition with An. bellator. Evolution. 1949, 4: 64-78. 10.2307/2405534.CrossRef Pittendrigh CS: The ectopic specialization of Anopheles homunculus, and its relation to competition with An. bellator. Evolution. 1949, 4: 64-78. 10.2307/2405534.CrossRef
2.
go back to reference Veloso HP, De Moura JV, Klein RM: Ecological limitation of Anopheles of the Subgenus Kerteszia in the coastal region of Southern Brazil. Mem Inst Oswaldo Cruz. 1956, 54: 517-548.PubMed Veloso HP, De Moura JV, Klein RM: Ecological limitation of Anopheles of the Subgenus Kerteszia in the coastal region of Southern Brazil. Mem Inst Oswaldo Cruz. 1956, 54: 517-548.PubMed
3.
go back to reference Rachou RG: Anofelinos do Brasil: Comportamento dasespécies vetoras de malária. Rev Bras Malariol Doencas Trop. 1958, 10: 145-181. Rachou RG: Anofelinos do Brasil: Comportamento dasespécies vetoras de malária. Rev Bras Malariol Doencas Trop. 1958, 10: 145-181.
4.
go back to reference Zavortink TJ: A review of the subgenus Kerteszia of Anopheles. Cont Am Entomol Inst. 1973, 9: 1-54. Zavortink TJ: A review of the subgenus Kerteszia of Anopheles. Cont Am Entomol Inst. 1973, 9: 1-54.
5.
go back to reference Consoli RAGB, Lourenço-de-Oliveira R: Principais mosquitos de importância sanitária no Brasil. 1994, Rio de Janeiro: Ed. Fiocruz Consoli RAGB, Lourenço-de-Oliveira R: Principais mosquitos de importância sanitária no Brasil. 1994, Rio de Janeiro: Ed. Fiocruz
6.
go back to reference Corrêa RR, Forattini OP, Guarita OF, Rabello EX: Observations on the flight of Anopheles (Kerteszia) cruzii and of A. (K.) bellator, vectors of malaria (Diptera, Culicidae). Arq Hig Saude Publica. 1961, 26: 333-342.PubMed Corrêa RR, Forattini OP, Guarita OF, Rabello EX: Observations on the flight of Anopheles (Kerteszia) cruzii and of A. (K.) bellator, vectors of malaria (Diptera, Culicidae). Arq Hig Saude Publica. 1961, 26: 333-342.PubMed
7.
go back to reference Aragão MB: Geographic distribution and abundance of Anopheles species (Kerteszia) (Diptera, Culicidae). Rev Bras Malariol Doencas Trop. 1964, 16: 73-109.PubMed Aragão MB: Geographic distribution and abundance of Anopheles species (Kerteszia) (Diptera, Culicidae). Rev Bras Malariol Doencas Trop. 1964, 16: 73-109.PubMed
8.
go back to reference Wilkerson RC, Peyton EL: The Brazilian malaria vector Anopheles (Kerteszia) cruzii: Life stages and biology (Diptera: Culicidae). Mosq Syst. 1991, 23: 110-122. Wilkerson RC, Peyton EL: The Brazilian malaria vector Anopheles (Kerteszia) cruzii: Life stages and biology (Diptera: Culicidae). Mosq Syst. 1991, 23: 110-122.
9.
go back to reference Forattini OP, Kakitani I, Massad E, Gomes Ade C: Studies on mosquitoes (Diptera: Culicidae) and anthropic environment. 1 – Parity of blood seeking Anopheles (Kerteszia) in south-eastern Brazil. Rev Saude Publica. 1993, 27: 1-8.CrossRefPubMed Forattini OP, Kakitani I, Massad E, Gomes Ade C: Studies on mosquitoes (Diptera: Culicidae) and anthropic environment. 1 – Parity of blood seeking Anopheles (Kerteszia) in south-eastern Brazil. Rev Saude Publica. 1993, 27: 1-8.CrossRefPubMed
10.
go back to reference Bona AC, Navarro-Silva MA: Anopheles cruzii parity in dense rain forest in Southern Brazil. Rev Saude Publica. 2006, 40: 1118-1123.CrossRefPubMed Bona AC, Navarro-Silva MA: Anopheles cruzii parity in dense rain forest in Southern Brazil. Rev Saude Publica. 2006, 40: 1118-1123.CrossRefPubMed
12.
go back to reference Machado RL, D' Almeida Couto AA, Cavasini CE, Calvosa VS: Malaria outside the Brazilian Amazonian region: the situation in Santa Catarina State. Rev Soc Bras Med Trop. 2003, 36: 581-586. 10.1590/S0037-86822003000500007.CrossRefPubMed Machado RL, D' Almeida Couto AA, Cavasini CE, Calvosa VS: Malaria outside the Brazilian Amazonian region: the situation in Santa Catarina State. Rev Soc Bras Med Trop. 2003, 36: 581-586. 10.1590/S0037-86822003000500007.CrossRefPubMed
14.
go back to reference Davis NC, Kumm HHW: Further incrimination of Anopheles darlingi Root as a transmitter of malaria. Am J Trop Med. 1932, 12: 93-95. Davis NC, Kumm HHW: Further incrimination of Anopheles darlingi Root as a transmitter of malaria. Am J Trop Med. 1932, 12: 93-95.
16.
go back to reference Rezende HR, Cerutti C, Santos CB: Aspectos atuais da distribuição geográfica de Anopheles (Kerteszia) cruzii Dyar & Knab, 1908 no Estado do Espírito Santo, Brasil. Entomol Vect. 2005, 12: 123-126.CrossRef Rezende HR, Cerutti C, Santos CB: Aspectos atuais da distribuição geográfica de Anopheles (Kerteszia) cruzii Dyar & Knab, 1908 no Estado do Espírito Santo, Brasil. Entomol Vect. 2005, 12: 123-126.CrossRef
17.
go back to reference Deane LM, Ferreira-Neto JA, Deane SP, Silveira IP: Anopheles (Kerteszia) cruzii, a natural vector of the monkey malaria parasites, Plasmodium simium and Plamodium brasilianum. Trans R Soc Trop Med Hyg. 1970, 64: 647-10.1016/0035-9203(70)90088-X.CrossRefPubMed Deane LM, Ferreira-Neto JA, Deane SP, Silveira IP: Anopheles (Kerteszia) cruzii, a natural vector of the monkey malaria parasites, Plasmodium simium and Plamodium brasilianum. Trans R Soc Trop Med Hyg. 1970, 64: 647-10.1016/0035-9203(70)90088-X.CrossRefPubMed
18.
go back to reference Marrelli MT, Malafronte RS, Sallum MA, Natal D: Kerteszia subgenus of Anopheles associated with the Brazilian Atlantic rainforest: current knowledge and future challenges. Malar J. 2007, 6: 127-134. 10.1186/1475-2875-6-127.PubMedCentralCrossRefPubMed Marrelli MT, Malafronte RS, Sallum MA, Natal D: Kerteszia subgenus of Anopheles associated with the Brazilian Atlantic rainforest: current knowledge and future challenges. Malar J. 2007, 6: 127-134. 10.1186/1475-2875-6-127.PubMedCentralCrossRefPubMed
19.
go back to reference Deane LM, Ferreira-Neto JA, Lima MM: The vertical dispersion of Anopheles (Kerteszia) cruzii in a forest in southern Brazil suggests that human cases of simian origin be expect. Mem Inst Oswaldo Cruz. 1984, 79: 461-463.CrossRefPubMed Deane LM, Ferreira-Neto JA, Lima MM: The vertical dispersion of Anopheles (Kerteszia) cruzii in a forest in southern Brazil suggests that human cases of simian origin be expect. Mem Inst Oswaldo Cruz. 1984, 79: 461-463.CrossRefPubMed
20.
go back to reference Ueno HM, Forattini OP, Kakitani I: Vertical and seasonal distribution of Anopheles (Kerteszia) in Ilha Comprida, Southeastern Brazil. Rev Saude Publica. 2007, 41: 269-275.CrossRefPubMed Ueno HM, Forattini OP, Kakitani I: Vertical and seasonal distribution of Anopheles (Kerteszia) in Ilha Comprida, Southeastern Brazil. Rev Saude Publica. 2007, 41: 269-275.CrossRefPubMed
21.
go back to reference Ramirez CC, Dessen EM: Cytogenetics analysis of a natural population of Anopheles cruzii. Rev Bras Genet. 1994, 17: 41-46. Ramirez CC, Dessen EM: Cytogenetics analysis of a natural population of Anopheles cruzii. Rev Bras Genet. 1994, 17: 41-46.
22.
go back to reference Ramirez CC, Dessen EM, Otto PA: Inversion polymorphism in a natural population of Anopheles cruzii. Caryologia. 1994, 47: 121-130.CrossRef Ramirez CC, Dessen EM, Otto PA: Inversion polymorphism in a natural population of Anopheles cruzii. Caryologia. 1994, 47: 121-130.CrossRef
23.
go back to reference Ramirez CC, Dessen EM: Chromosomal evidence for sibling species of the malaria vector Anopheles cruzii. Genome. 2000, 43: 143-151. 10.1139/gen-43-1-143.CrossRefPubMed Ramirez CC, Dessen EM: Chromosomal evidence for sibling species of the malaria vector Anopheles cruzii. Genome. 2000, 43: 143-151. 10.1139/gen-43-1-143.CrossRefPubMed
24.
go back to reference Ramirez CC, Dessen EM: Chromosome differentiated populations of Anopheles cruzii: evidence for a third sibling species. Genetica. 2000, 108: 73-80. 10.1023/A:1004020904877.CrossRefPubMed Ramirez CC, Dessen EM: Chromosome differentiated populations of Anopheles cruzii: evidence for a third sibling species. Genetica. 2000, 108: 73-80. 10.1023/A:1004020904877.CrossRefPubMed
25.
go back to reference Carvalho-Pinto CJ, Lourenço-de-Oliveira R: Isoenzymatic analysis of four Anopheles (Kerteszia) cruzii (Díptera: Culicidae) populations of Brazil. Mem Inst Oswaldo Cruz. 2004, 99: 471-475. 10.1590/S0074-02762004000500002.CrossRefPubMed Carvalho-Pinto CJ, Lourenço-de-Oliveira R: Isoenzymatic analysis of four Anopheles (Kerteszia) cruzii (Díptera: Culicidae) populations of Brazil. Mem Inst Oswaldo Cruz. 2004, 99: 471-475. 10.1590/S0074-02762004000500002.CrossRefPubMed
26.
go back to reference Malafronte Rdos S, Marrelli MT, Ramirez CC, Nassar MN, Marinotti O: Intraspecific variation of second internal transcribed spacer of nuclear ribosomal DNA among populations of Anopheles (Kerteszia) cruzii (Diptera: Culicidae). J Med Entomol. 2007, 44: 538-542. 10.1603/0022-2585(2007)44[538:IVOSIT]2.0.CO;2.CrossRefPubMed Malafronte Rdos S, Marrelli MT, Ramirez CC, Nassar MN, Marinotti O: Intraspecific variation of second internal transcribed spacer of nuclear ribosomal DNA among populations of Anopheles (Kerteszia) cruzii (Diptera: Culicidae). J Med Entomol. 2007, 44: 538-542. 10.1603/0022-2585(2007)44[538:IVOSIT]2.0.CO;2.CrossRefPubMed
27.
go back to reference Hardin PE: The Circadian Timekeeping System of Drosophila. Curr Biol. 2005, 15: 714-722. 10.1016/j.cub.2005.08.019.CrossRef Hardin PE: The Circadian Timekeeping System of Drosophila. Curr Biol. 2005, 15: 714-722. 10.1016/j.cub.2005.08.019.CrossRef
28.
go back to reference Sakai T, Ishida N: Circadian rhythms of female mating activity governed by clock genes in Drosophila. Proc Natl Acad Sci. 2001, 98: 9221-9225. 10.1073/pnas.151443298.PubMedCentralCrossRefPubMed Sakai T, Ishida N: Circadian rhythms of female mating activity governed by clock genes in Drosophila. Proc Natl Acad Sci. 2001, 98: 9221-9225. 10.1073/pnas.151443298.PubMedCentralCrossRefPubMed
29.
go back to reference Tauber E, Roe H, Costa R, Hennessy JM, Kyriacou CP: Temporal mating isolation driven by a behavioral gene in Drosophila. Curr Biol. 2003, 13: 140-145. 10.1016/S0960-9822(03)00004-6.CrossRefPubMed Tauber E, Roe H, Costa R, Hennessy JM, Kyriacou CP: Temporal mating isolation driven by a behavioral gene in Drosophila. Curr Biol. 2003, 13: 140-145. 10.1016/S0960-9822(03)00004-6.CrossRefPubMed
30.
go back to reference Pittendrigh CS: The quantitative evaluation of Kerteszia breeding grounds. Am J Trop Med Hyg. 1950, 30: 457-468.PubMed Pittendrigh CS: The quantitative evaluation of Kerteszia breeding grounds. Am J Trop Med Hyg. 1950, 30: 457-468.PubMed
31.
go back to reference Chahad-Ehlers S, Lozovei AL, Marques MD: Reproductive and post-embryonic daily rhythm patterns of the malaria vector Anopheles (Kerteszia) cruzii: aspects of the life cycle. Chronobiol Int. 2007, 24: 289-304. 10.1080/07420520701282174.CrossRefPubMed Chahad-Ehlers S, Lozovei AL, Marques MD: Reproductive and post-embryonic daily rhythm patterns of the malaria vector Anopheles (Kerteszia) cruzii: aspects of the life cycle. Chronobiol Int. 2007, 24: 289-304. 10.1080/07420520701282174.CrossRefPubMed
32.
go back to reference Jowett T: Preparation of nucleic acids. Drosophila, A Practical Approach. 1998, IRL press, Oxford: Roberts DB, 347-371. Jowett T: Preparation of nucleic acids. Drosophila, A Practical Approach. 1998, IRL press, Oxford: Roberts DB, 347-371.
33.
go back to reference Gentile C, Meireles-Filho AC, Britto C, Lima JB, Valle D, Peixoto AA: Cloning and daily expression of the timeless gene in Aedes aegypti (Diptera:Culicidae). Insect Biochem Mol Biol. 2006, 36: 878-884. 10.1016/j.ibmb.2006.08.008.CrossRefPubMed Gentile C, Meireles-Filho AC, Britto C, Lima JB, Valle D, Peixoto AA: Cloning and daily expression of the timeless gene in Aedes aegypti (Diptera:Culicidae). Insect Biochem Mol Biol. 2006, 36: 878-884. 10.1016/j.ibmb.2006.08.008.CrossRefPubMed
35.
go back to reference Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG: The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 25: 4876-4882. 10.1093/nar/25.24.4876.PubMedCentralCrossRefPubMed Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG: The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 25: 4876-4882. 10.1093/nar/25.24.4876.PubMedCentralCrossRefPubMed
36.
go back to reference Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R: DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics. 2003, 19: 2496-2497. 10.1093/bioinformatics/btg359.CrossRefPubMed Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R: DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics. 2003, 19: 2496-2497. 10.1093/bioinformatics/btg359.CrossRefPubMed
37.
go back to reference Filatov DA, Charlesworth D: DNA polimorphism, haplotype structure and balancing selection in the Leavenworthia PgiC locus. Genetics. 1999, 153: 1423-1434.PubMedCentralPubMed Filatov DA, Charlesworth D: DNA polimorphism, haplotype structure and balancing selection in the Leavenworthia PgiC locus. Genetics. 1999, 153: 1423-1434.PubMedCentralPubMed
38.
go back to reference Hudson RR, Slatkin M, Maddison WP: Estimation of levels of gene flow from DNA sequence data. Genetics. 1992, 132: 583-589.PubMedCentralPubMed Hudson RR, Slatkin M, Maddison WP: Estimation of levels of gene flow from DNA sequence data. Genetics. 1992, 132: 583-589.PubMedCentralPubMed
39.
go back to reference Tamura K, Dudley J, Nei M, Kumar S: MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol. 2007, 24: 1596-1599. 10.1093/molbev/msm092.CrossRefPubMed Tamura K, Dudley J, Nei M, Kumar S: MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol. 2007, 24: 1596-1599. 10.1093/molbev/msm092.CrossRefPubMed
40.
go back to reference Tajima F: Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989, 123: 585-595.PubMedCentralPubMed Tajima F: Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989, 123: 585-595.PubMedCentralPubMed
42.
go back to reference Tamura K, Subramanian S, Kumar S: Temporal Patterns of Fruit Fly (Drosophila) Evolution Revealed by Mutation Clocks. Mol Biol Evol. 2004, 21 (1): 36-44. 10.1093/molbev/msg236.CrossRefPubMed Tamura K, Subramanian S, Kumar S: Temporal Patterns of Fruit Fly (Drosophila) Evolution Revealed by Mutation Clocks. Mol Biol Evol. 2004, 21 (1): 36-44. 10.1093/molbev/msg236.CrossRefPubMed
43.
44.
go back to reference Calado DC, Navarro-Silva MA, Sallum MAM: PCR-RAPD and PCR-RFLP polymorphism detected in Anopheles cruzii (Diptera, Culicidae). Rev Bras Entomol. 2006, 50: 423-430. 10.1590/S0085-56262006000300014.CrossRef Calado DC, Navarro-Silva MA, Sallum MAM: PCR-RAPD and PCR-RFLP polymorphism detected in Anopheles cruzii (Diptera, Culicidae). Rev Bras Entomol. 2006, 50: 423-430. 10.1590/S0085-56262006000300014.CrossRef
45.
go back to reference Vasconcelos PM, Becker TA, Renne PR, Brimhall GH: Age and duration of weathering by 40K-40Ar and 40Ar/39Ar analysis of potassium-manganese oxides. Science. 1992, 258: 451-455. 10.1126/science.258.5081.451.CrossRefPubMed Vasconcelos PM, Becker TA, Renne PR, Brimhall GH: Age and duration of weathering by 40K-40Ar and 40Ar/39Ar analysis of potassium-manganese oxides. Science. 1992, 258: 451-455. 10.1126/science.258.5081.451.CrossRefPubMed
46.
go back to reference Marroig G, Cropp S, Cheverud JM: Systematics and evolution of the Jacchus group of marmosets (Platyrrhini). Am J Phys Anthropol. 2004, 123: 11-22. 10.1002/ajpa.10146.CrossRefPubMed Marroig G, Cropp S, Cheverud JM: Systematics and evolution of the Jacchus group of marmosets (Platyrrhini). Am J Phys Anthropol. 2004, 123: 11-22. 10.1002/ajpa.10146.CrossRefPubMed
47.
go back to reference Carnaval AC, Hickerson MJ, Haddad CF, Rodrigues MT, Moritz C: Stability predicts genetic diversity in the Brazilian Atlantic forest hotspot. Science. 2009, 323: 785-789. 10.1126/science.1166955.CrossRefPubMed Carnaval AC, Hickerson MJ, Haddad CF, Rodrigues MT, Moritz C: Stability predicts genetic diversity in the Brazilian Atlantic forest hotspot. Science. 2009, 323: 785-789. 10.1126/science.1166955.CrossRefPubMed
48.
go back to reference Pedro PM, Sallum MA, Butlin RK: Forest-obligate Sabethes mosquitoes suggest palaeoecological perturbations. Heredity. 2008, 101: 186-95. 10.1038/hdy.2008.45.CrossRefPubMed Pedro PM, Sallum MA, Butlin RK: Forest-obligate Sabethes mosquitoes suggest palaeoecological perturbations. Heredity. 2008, 101: 186-95. 10.1038/hdy.2008.45.CrossRefPubMed
49.
go back to reference Nei M, Kumar S: Molecular Evolution and Phylogenetics. 2000, New York: Oxford University Press Nei M, Kumar S: Molecular Evolution and Phylogenetics. 2000, New York: Oxford University Press
Metadata
Title
Assessing the molecular divergence between Anopheles (Kerteszia) cruzii populations from Brazil using the timeless gene: further evidence of a species complex
Authors
Luísa DP Rona
Carlos J Carvalho-Pinto
Carla Gentile
Edmundo C Grisard
Alexandre A Peixoto
Publication date
01-12-2009
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2009
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-8-60

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