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Published in: Malaria Journal 1/2010

Open Access 01-12-2010 | Research

Complete mtDNA genomes of Anopheles darlingi and an approach to anopheline divergence time

Authors: Marta Moreno, Osvaldo Marinotti, Jaroslaw Krzywinski, Wanderli P Tadei, Anthony A James, Nicole L Achee, Jan E Conn

Published in: Malaria Journal | Issue 1/2010

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Abstract

Background

The complete sequences of the mitochondrial genomes (mtDNA) of members of the northern and southern genotypes of Anopheles (Nyssorhynchus) darlingi were used for comparative studies to estimate the time to the most recent common ancestor for modern anophelines, to evaluate differentiation within this taxon, and to seek evidence of incipient speciation.

Methods

The mtDNAs were sequenced from mosquitoes from Belize and Brazil and comparative analyses of structure and base composition, among others, were performed. A maximum likelihood approach linked with phylogenetic information was employed to detect evidence of selection and a Bayesian approach was used to date the split between the subgenus Nyssorhynchus and other Anopheles subgenera.

Results

The comparison of mtDNA sequences within the Anopheles darlingi taxon does not provide sufficient resolution to establish different units of speciation within the species. In addition, no evidence of positive selection in any protein-coding gene of the mtDNA was detected, and purifying selection likely is the basis for this lack of diversity. Bayesian analysis supports the conclusion that the most recent ancestor of Nyssorhynchus and Anopheles+Cellia was extant ~94 million years ago.

Conclusion

Analyses of mtDNA genomes of Anopheles darlingi do not provide support for speciation in the taxon. The dates estimated for divergence among the anopheline groups tested is in agreement with the geological split of western Gondwana (95 mya), and provides additional support for explaining the absence of Cellia in the New World, and Nyssorhynchus in the Afro-Eurasian continents.
Appendix
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Literature
1.
go back to reference World Health Organization: World Malaria Report 2008. 2008, WHO. Geneva, HO/HTM/GMP/2008.1CrossRef World Health Organization: World Malaria Report 2008. 2008, WHO. Geneva, HO/HTM/GMP/2008.1CrossRef
2.
go back to reference Linthicum KJ: A revision of the Argyritarsis section of the subgenus Nyssorhynchus of Anopheles (Diptera: Culicidae). Mosq Syst. 1988, 20: 98-271. Linthicum KJ: A revision of the Argyritarsis section of the subgenus Nyssorhynchus of Anopheles (Diptera: Culicidae). Mosq Syst. 1988, 20: 98-271.
3.
go back to reference Charlwood JD: Biological variation in Anopheles darlingi Root. Mem Inst Oswaldo Cruz. 1996, 91: 391-398.PubMed Charlwood JD: Biological variation in Anopheles darlingi Root. Mem Inst Oswaldo Cruz. 1996, 91: 391-398.PubMed
4.
go back to reference Lounibos LP, Conn JE: Malaria vector heterogeneity in South America. American Entomologist. 2000, 46: 238-249.CrossRef Lounibos LP, Conn JE: Malaria vector heterogeneity in South America. American Entomologist. 2000, 46: 238-249.CrossRef
5.
go back to reference Zimmerman RH, Galardo AK, Lounibos LP, Arruda M, Wirtz R: Bloodmeal hosts of Anopheles species (Diptera: Culicidae) in a malaria-endemic area of the Brazilian Amazon. J Med Entomol. 2006, 43: 947-956. 10.1603/0022-2585(2006)43[947:BHOASD]2.0.CO;2.CrossRefPubMed Zimmerman RH, Galardo AK, Lounibos LP, Arruda M, Wirtz R: Bloodmeal hosts of Anopheles species (Diptera: Culicidae) in a malaria-endemic area of the Brazilian Amazon. J Med Entomol. 2006, 43: 947-956. 10.1603/0022-2585(2006)43[947:BHOASD]2.0.CO;2.CrossRefPubMed
6.
go back to reference Tadei WP, Santos JMM, Rabbani MG: Biologia de anofelinos amazônicos. V. Polimorfismo cromossômico de Anopheles darlingi Root (Diptera: Culicidae). Acta Amazonica. 1982, 12: 353-369. Tadei WP, Santos JMM, Rabbani MG: Biologia de anofelinos amazônicos. V. Polimorfismo cromossômico de Anopheles darlingi Root (Diptera: Culicidae). Acta Amazonica. 1982, 12: 353-369.
7.
go back to reference Steiner WWM, Narang S, Kitzmiller JB, Swofford DL: Genetic divergence and evolution in Neotropical Anopheles (subgenus Nyssorhynchus). Recent developments in the genetics of insect disease vectors. Edited by: Steiner WWM, Tabachnick WJ, Rai KS, Narang S. 1982, Stipes Champaign, Illinois, 523-551. Steiner WWM, Narang S, Kitzmiller JB, Swofford DL: Genetic divergence and evolution in Neotropical Anopheles (subgenus Nyssorhynchus). Recent developments in the genetics of insect disease vectors. Edited by: Steiner WWM, Tabachnick WJ, Rai KS, Narang S. 1982, Stipes Champaign, Illinois, 523-551.
8.
go back to reference Malafronte RS, Marrelli MT, Marinotti O: Analysis of ITS2 DNA sequences from Brazilian Anopheles darlingi (Diptera: Culicidae). J Med Entomol. 1999, 36: 631-634.CrossRefPubMed Malafronte RS, Marrelli MT, Marinotti O: Analysis of ITS2 DNA sequences from Brazilian Anopheles darlingi (Diptera: Culicidae). J Med Entomol. 1999, 36: 631-634.CrossRefPubMed
9.
go back to reference Manguin S, Wilkerson RC, Conn JE, Rubio-Palis Y, Danoff-Burg JA, Roberts DR: Population structure of the primary malaria vector in South America, Anopheles darlingi, using isozyme, random amplified polymorphic DNA, internal transcribed spacer 2, and morphologic markers. Am J Trop Med Hyg. 1999, 60: 364-376.PubMed Manguin S, Wilkerson RC, Conn JE, Rubio-Palis Y, Danoff-Burg JA, Roberts DR: Population structure of the primary malaria vector in South America, Anopheles darlingi, using isozyme, random amplified polymorphic DNA, internal transcribed spacer 2, and morphologic markers. Am J Trop Med Hyg. 1999, 60: 364-376.PubMed
10.
go back to reference Mirabello L, Conn JE: Molecular population genetics of the malaria vector Anopheles darlingi in Central and South America. Heredity. 2006, 96: 311-321. 10.1038/sj.hdy.6800805.CrossRefPubMed Mirabello L, Conn JE: Molecular population genetics of the malaria vector Anopheles darlingi in Central and South America. Heredity. 2006, 96: 311-321. 10.1038/sj.hdy.6800805.CrossRefPubMed
11.
go back to reference Conn JE, Vineis JH, Bollback JP, Onyabe DY, Wilkerson RC, Povoa MM: Population structure of the malaria vector Anopheles darlingi in a malaria-endemic region of eastern Amazonian Brazil. Am J Trop Med Hyg. 2006, 74: 798-806.PubMed Conn JE, Vineis JH, Bollback JP, Onyabe DY, Wilkerson RC, Povoa MM: Population structure of the malaria vector Anopheles darlingi in a malaria-endemic region of eastern Amazonian Brazil. Am J Trop Med Hyg. 2006, 74: 798-806.PubMed
12.
go back to reference Mirabello L, Vineis JH, Yanoviak SP, Scarpassa VM, Povoa MM, Padilla N, Achee NL, Conn JE: Microsatellite data suggest significant population structure and differentiation within the malaria vector Anopheles darlingi in Central and South America. BMC Ecol. 2008, 8: 3-10.1186/1472-6785-8-3.PubMedCentralCrossRefPubMed Mirabello L, Vineis JH, Yanoviak SP, Scarpassa VM, Povoa MM, Padilla N, Achee NL, Conn JE: Microsatellite data suggest significant population structure and differentiation within the malaria vector Anopheles darlingi in Central and South America. BMC Ecol. 2008, 8: 3-10.1186/1472-6785-8-3.PubMedCentralCrossRefPubMed
13.
go back to reference Pedro P, Sallum MAM: Spatial expansion and population structure of the neotropical malaria vector, Anopheles darlingi. Biol J Linnean Soc. 2009, 97: 854-866. 10.1111/j.1095-8312.2009.01226.x.CrossRef Pedro P, Sallum MAM: Spatial expansion and population structure of the neotropical malaria vector, Anopheles darlingi. Biol J Linnean Soc. 2009, 97: 854-866. 10.1111/j.1095-8312.2009.01226.x.CrossRef
14.
go back to reference Mirabello L: Molecular population genetics of the malaria vector Anopheles darlingi throughout Central and South America using mitochondrial, nuclear, and microsatellite markers. PhD thesis. 2007, State University of New York at Albany, Biomedical Sciences Department Mirabello L: Molecular population genetics of the malaria vector Anopheles darlingi throughout Central and South America using mitochondrial, nuclear, and microsatellite markers. PhD thesis. 2007, State University of New York at Albany, Biomedical Sciences Department
15.
go back to reference Boore JL, Collins TM, Stanton D, Daehler LL, Brown WM: Deducing the pattern of arthropod phylogeny from mitochondrial DNA rearrangements. Nature. 1995, 376: 163-165. 10.1038/376163a0.CrossRefPubMed Boore JL, Collins TM, Stanton D, Daehler LL, Brown WM: Deducing the pattern of arthropod phylogeny from mitochondrial DNA rearrangements. Nature. 1995, 376: 163-165. 10.1038/376163a0.CrossRefPubMed
16.
go back to reference Boore JL, Macey JR, Medina M: Sequencing and comparing whole mitochondrial genomes of animals. Methods Enzymol. 2005, 395: 311-348. full_text.CrossRefPubMed Boore JL, Macey JR, Medina M: Sequencing and comparing whole mitochondrial genomes of animals. Methods Enzymol. 2005, 395: 311-348. full_text.CrossRefPubMed
17.
go back to reference Mitchell SE, Cockburn AF, Seawright JA: The mitochondrial genome of Anopheles quadrimaculatus species A: complete nucleotide sequence and gene organization. Genome. 1993, 36: 1058-1073. 10.1139/g93-141.CrossRefPubMed Mitchell SE, Cockburn AF, Seawright JA: The mitochondrial genome of Anopheles quadrimaculatus species A: complete nucleotide sequence and gene organization. Genome. 1993, 36: 1058-1073. 10.1139/g93-141.CrossRefPubMed
18.
go back to reference Beard CB, Hamm DM, Collins FH: The mitochondrial genome of the mosquito Anopheles gambiae: DNA sequence, genome organization, and comparisons with mitochondrial sequences of other insects. Insect Mol Biol. 1993, 2: 103-124. 10.1111/j.1365-2583.1993.tb00131.x.CrossRefPubMed Beard CB, Hamm DM, Collins FH: The mitochondrial genome of the mosquito Anopheles gambiae: DNA sequence, genome organization, and comparisons with mitochondrial sequences of other insects. Insect Mol Biol. 1993, 2: 103-124. 10.1111/j.1365-2583.1993.tb00131.x.CrossRefPubMed
19.
go back to reference Krzywinski J, Grushko OG, Besansky NJ: Analysis of the complete mitochondrial DNA from Anopheles funestus: an improved dipteran mitochondrial genome annotation and a temporal dimension of mosquito evolution. Mol Phylogenet Evol. 2006, 39: 417-423. 10.1016/j.ympev.2006.01.006.CrossRefPubMed Krzywinski J, Grushko OG, Besansky NJ: Analysis of the complete mitochondrial DNA from Anopheles funestus: an improved dipteran mitochondrial genome annotation and a temporal dimension of mosquito evolution. Mol Phylogenet Evol. 2006, 39: 417-423. 10.1016/j.ympev.2006.01.006.CrossRefPubMed
20.
go back to reference Bazin E, Glemin S, Galtier N: Population size does not influence mitochondrial genetic diversity in animals. Science. 2006, 312: 570-572. 10.1126/science.1122033.CrossRefPubMed Bazin E, Glemin S, Galtier N: Population size does not influence mitochondrial genetic diversity in animals. Science. 2006, 312: 570-572. 10.1126/science.1122033.CrossRefPubMed
21.
go back to reference Meiklejohn CD, Montooth KL, Rand DM: Positive and negative selection on the mitochondrial genome. Trends Genet. 2007, 23: 259-63. 10.1016/j.tig.2007.03.008.CrossRefPubMed Meiklejohn CD, Montooth KL, Rand DM: Positive and negative selection on the mitochondrial genome. Trends Genet. 2007, 23: 259-63. 10.1016/j.tig.2007.03.008.CrossRefPubMed
22.
go back to reference Conn JE, Mirabello L: The biogeography and population genetics of neotropical vector species. Heredity. 2007, 99: 245-256. 10.1038/sj.hdy.6801002.CrossRefPubMed Conn JE, Mirabello L: The biogeography and population genetics of neotropical vector species. Heredity. 2007, 99: 245-256. 10.1038/sj.hdy.6801002.CrossRefPubMed
23.
go back to reference Foley DH, Wilkerson RC, Cooper RD, Volovsek ME, Bryan JH: A molecular phylogeny of Anopheles annulipes (Diptera: Culicidae) sensu lato: the most species-rich anopheline complex. Mol Phylogenet Evol. 2007, 43: 283-297. 10.1016/j.ympev.2006.10.008.CrossRefPubMed Foley DH, Wilkerson RC, Cooper RD, Volovsek ME, Bryan JH: A molecular phylogeny of Anopheles annulipes (Diptera: Culicidae) sensu lato: the most species-rich anopheline complex. Mol Phylogenet Evol. 2007, 43: 283-297. 10.1016/j.ympev.2006.10.008.CrossRefPubMed
24.
go back to reference Morgan K, O'Loughlin SM, Mun-Yik F, Linton YM, Somboon P, Min S, Htun PT, Nambanya S, Weerasinghe I, Sochantha T, Prakash A, Walton C: Molecular phylogenetics and biogeography of the Neocellia Series of Anopheles mosquitoes in the oriental region. Mol Phylogenet Evol. 2009, 52: 588-601. 10.1016/j.ympev.2009.01.022.CrossRefPubMed Morgan K, O'Loughlin SM, Mun-Yik F, Linton YM, Somboon P, Min S, Htun PT, Nambanya S, Weerasinghe I, Sochantha T, Prakash A, Walton C: Molecular phylogenetics and biogeography of the Neocellia Series of Anopheles mosquitoes in the oriental region. Mol Phylogenet Evol. 2009, 52: 588-601. 10.1016/j.ympev.2009.01.022.CrossRefPubMed
25.
go back to reference Krzywinski J, Besansky NJ: Molecular systematics of Anopheles: from subgenera to subpopulations. Annu Rev Entomol. 2003, 48: 111-139. 10.1146/annurev.ento.48.091801.112647.CrossRefPubMed Krzywinski J, Besansky NJ: Molecular systematics of Anopheles: from subgenera to subpopulations. Annu Rev Entomol. 2003, 48: 111-139. 10.1146/annurev.ento.48.091801.112647.CrossRefPubMed
26.
go back to reference Wilkerson RC, Strickman D: Illustrated key to the female Anophelinae mosquitoes of Central America and Mexico. J Am Mosq Control Assoc. 1990, 6: 7-34.PubMed Wilkerson RC, Strickman D: Illustrated key to the female Anophelinae mosquitoes of Central America and Mexico. J Am Mosq Control Assoc. 1990, 6: 7-34.PubMed
27.
go back to reference Faran ME, Linthicum KJ: A handbook of Amazonian species of Anopheles (Nyssorhynchus) (Diptera: Culicidae). Mosq Syst. 1981, 8: 1-107. Faran ME, Linthicum KJ: A handbook of Amazonian species of Anopheles (Nyssorhynchus) (Diptera: Culicidae). Mosq Syst. 1981, 8: 1-107.
28.
go back to reference Forattini OP: Entomologia Médica. 1962, São Paulo: Universidade São Paulo, I: Forattini OP: Entomologia Médica. 1962, São Paulo: Universidade São Paulo, I:
29.
go back to reference Rozen S, Skaletsky H: Primer3 on the www for general users and for biologist programmers. Methods Mol Biol. 2000, 132: 365-386.PubMed Rozen S, Skaletsky H: Primer3 on the www for general users and for biologist programmers. Methods Mol Biol. 2000, 132: 365-386.PubMed
31.
go back to reference Lowe TM, Eddy SR: tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 1997, 25: 955-64. 10.1093/nar/25.5.955.PubMedCentralCrossRefPubMed Lowe TM, Eddy SR: tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 1997, 25: 955-64. 10.1093/nar/25.5.955.PubMedCentralCrossRefPubMed
32.
go back to reference Kumar S, Tamura K, Nei M: MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform. 2004, 5: 150-163. 10.1093/bib/5.2.150.CrossRefPubMed Kumar S, Tamura K, Nei M: MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform. 2004, 5: 150-163. 10.1093/bib/5.2.150.CrossRefPubMed
33.
go back to reference Perna NT, Kocher TD: Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. J Mol Evol. 1995, 41: 353-358. 10.1007/BF01215182.CrossRefPubMed Perna NT, Kocher TD: Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. J Mol Evol. 1995, 41: 353-358. 10.1007/BF01215182.CrossRefPubMed
34.
go back to reference Rozas J, Sanchez-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, Sanchez-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
35.
go back to reference Xia X, Xie Z: DAMBE: software package for data analysis in molecular biology and evolution. J Hered. 2001, 92: 371-373. 10.1093/jhered/92.4.371.CrossRefPubMed Xia X, Xie Z: DAMBE: software package for data analysis in molecular biology and evolution. J Hered. 2001, 92: 371-373. 10.1093/jhered/92.4.371.CrossRefPubMed
36.
go back to reference Kolpakov R, Bana G, Kucherov G: mreps: Efficient and flexible detection of tandem repeats in DNA. Nucleic Acids Res. 2003, 31: 3672-3678. 10.1093/nar/gkg617.PubMedCentralCrossRefPubMed Kolpakov R, Bana G, Kucherov G: mreps: Efficient and flexible detection of tandem repeats in DNA. Nucleic Acids Res. 2003, 31: 3672-3678. 10.1093/nar/gkg617.PubMedCentralCrossRefPubMed
37.
go back to reference Nei M, Gojobori T: Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986, 3: 418-426.PubMed Nei M, Gojobori T: Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986, 3: 418-426.PubMed
38.
go back to reference Yang Z: PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci. 1997, 13: 555-556.PubMed Yang Z: PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci. 1997, 13: 555-556.PubMed
39.
go back to reference Yang Z, Nielsen R: Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol. 2002, 19: 908-917.CrossRefPubMed Yang Z, Nielsen R: Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol. 2002, 19: 908-917.CrossRefPubMed
40.
go back to reference Yang Z, Wong WSW, Nielsen R: Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol. 2005, 22: 1107-1118. 10.1093/molbev/msi097.CrossRefPubMed Yang Z, Wong WSW, Nielsen R: Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol. 2005, 22: 1107-1118. 10.1093/molbev/msi097.CrossRefPubMed
41.
go back to reference Zhang J, Nielsen R, Yang Z: Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol. 2005, 22: 2472-2479. 10.1093/molbev/msi237.CrossRefPubMed Zhang J, Nielsen R, Yang Z: Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol. 2005, 22: 2472-2479. 10.1093/molbev/msi237.CrossRefPubMed
42.
go back to reference Swofford DL: PAUP* version 4.0b10. Phylogenetic Analysis Using Parsimony (*and Other Methods). 2000, Sinauer Associates, Inc, Sunderland, Massachusetts, USA Swofford DL: PAUP* version 4.0b10. Phylogenetic Analysis Using Parsimony (*and Other Methods). 2000, Sinauer Associates, Inc, Sunderland, Massachusetts, USA
43.
go back to reference Clary DO, Wolstenholme DR: The mitochondrial DNA molecular of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol. 1985, 22: 252-271. 10.1007/BF02099755.CrossRefPubMed Clary DO, Wolstenholme DR: The mitochondrial DNA molecular of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol. 1985, 22: 252-271. 10.1007/BF02099755.CrossRefPubMed
44.
go back to reference Swofford DL, Olsen GJ, Waddell PJ, Hillis DM: Phylogenetic inference. Molecular systematics. Edited by: Hillis DM, Moritz C, Mable BK. 1996, Sinauer, Sunderland, Mass, 407-514. 2 Swofford DL, Olsen GJ, Waddell PJ, Hillis DM: Phylogenetic inference. Molecular systematics. Edited by: Hillis DM, Moritz C, Mable BK. 1996, Sinauer, Sunderland, Mass, 407-514. 2
45.
go back to reference Posada D, Crandall KA: MODELTEST: testing the model of DNA substitution. Bioinformatics. 1998, 14: 817-818. 10.1093/bioinformatics/14.9.817.CrossRefPubMed Posada D, Crandall KA: MODELTEST: testing the model of DNA substitution. Bioinformatics. 1998, 14: 817-818. 10.1093/bioinformatics/14.9.817.CrossRefPubMed
46.
go back to reference Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003, 19: 1572-1574. 10.1093/bioinformatics/btg180.CrossRefPubMed Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003, 19: 1572-1574. 10.1093/bioinformatics/btg180.CrossRefPubMed
47.
go back to reference Zavortink TJ, Poinar GO: Anopheles (Nyssorhynchus) dominicanus sp. n. (Diptera: Culicidae) from Dominican amber. Ann Entomol Soc Am. 2000, 93: 1230-1235. 10.1603/0013-8746(2000)093[1230:ANDSND]2.0.CO;2.CrossRef Zavortink TJ, Poinar GO: Anopheles (Nyssorhynchus) dominicanus sp. n. (Diptera: Culicidae) from Dominican amber. Ann Entomol Soc Am. 2000, 93: 1230-1235. 10.1603/0013-8746(2000)093[1230:ANDSND]2.0.CO;2.CrossRef
48.
go back to reference Iturralde-Vincent MA, MacPhee RDE: Age and paleogeographical origin of Dominican amber. Science. 1996, 273: 1850-1852. 10.1126/science.273.5283.1850.CrossRef Iturralde-Vincent MA, MacPhee RDE: Age and paleogeographical origin of Dominican amber. Science. 1996, 273: 1850-1852. 10.1126/science.273.5283.1850.CrossRef
49.
go back to reference Schlee D: Das Bernstein-Kabinett. Sttutg Beitr Naturk C. 1990, 28: 100- Schlee D: Das Bernstein-Kabinett. Sttutg Beitr Naturk C. 1990, 28: 100-
50.
go back to reference Gaunt MW, Miles MA: An insect molecular clock dates the origin of the insects and accords with palaeontological and biogeographic landmarks. Mol Biol Evol. 2002, 19: 748-761.CrossRefPubMed Gaunt MW, Miles MA: An insect molecular clock dates the origin of the insects and accords with palaeontological and biogeographic landmarks. Mol Biol Evol. 2002, 19: 748-761.CrossRefPubMed
51.
go back to reference Ho SY, Larson G: Molecular clocks: when times are a-changin'. Trends Genet. 2006, 22 (2): 79-83. 10.1016/j.tig.2005.11.006.CrossRefPubMed Ho SY, Larson G: Molecular clocks: when times are a-changin'. Trends Genet. 2006, 22 (2): 79-83. 10.1016/j.tig.2005.11.006.CrossRefPubMed
52.
go back to reference Brower AV: Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proc Natl Acad Sci USA. 1994, 91: 6491-6495. 10.1073/pnas.91.14.6491.PubMedCentralCrossRefPubMed Brower AV: Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proc Natl Acad Sci USA. 1994, 91: 6491-6495. 10.1073/pnas.91.14.6491.PubMedCentralCrossRefPubMed
53.
go back to reference DeSalle R, Templeton A, Mori I, Pletscher S, Johnston JS: Temporal and spatial heterogeneity of mtDNA polymorphisms in natural populations of Drosophila mercatorum. Genetics. 1987, 116: 215-23.PubMedCentralPubMed DeSalle R, Templeton A, Mori I, Pletscher S, Johnston JS: Temporal and spatial heterogeneity of mtDNA polymorphisms in natural populations of Drosophila mercatorum. Genetics. 1987, 116: 215-23.PubMedCentralPubMed
55.
56.
go back to reference Stewart JB, Beckenbach AT: Insect mitochondrial genomics: the complete mitochondrial genome sequence of the meadow spittlebug Philaenus spumarius (Hemiptera: Auchenorrhyncha: Cercopoidae). Genome. 2005, 48: 46-54. 10.1139/g04-090.CrossRefPubMed Stewart JB, Beckenbach AT: Insect mitochondrial genomics: the complete mitochondrial genome sequence of the meadow spittlebug Philaenus spumarius (Hemiptera: Auchenorrhyncha: Cercopoidae). Genome. 2005, 48: 46-54. 10.1139/g04-090.CrossRefPubMed
57.
go back to reference Saccone C, De GC, Gissi C, Pesole G, Reyes A: Evolutionary genomics in Metazoa: the mitochondrial DNA as a model system. Gene. 1999, 238: 195-209. 10.1016/S0378-1119(99)00270-X.CrossRefPubMed Saccone C, De GC, Gissi C, Pesole G, Reyes A: Evolutionary genomics in Metazoa: the mitochondrial DNA as a model system. Gene. 1999, 238: 195-209. 10.1016/S0378-1119(99)00270-X.CrossRefPubMed
58.
go back to reference Junqueira AC, Lessinger AC, Torres TT, da Silva FR, Vettore AL, Arruda P, Zeredo Espin AM: The mitochondrial genome of the blowfly Chrysomya chloropyga (Diptera: Calliphoridae). Gene. 2004, 339: 7-15. 10.1016/j.gene.2004.06.031.CrossRefPubMed Junqueira AC, Lessinger AC, Torres TT, da Silva FR, Vettore AL, Arruda P, Zeredo Espin AM: The mitochondrial genome of the blowfly Chrysomya chloropyga (Diptera: Calliphoridae). Gene. 2004, 339: 7-15. 10.1016/j.gene.2004.06.031.CrossRefPubMed
59.
go back to reference Ojala D, Montoya J, Attardi G: tRNA punctuation model of RNA processing in human mitochondria. Nature. 1981, 290: 470-474. 10.1038/290470a0.CrossRefPubMed Ojala D, Montoya J, Attardi G: tRNA punctuation model of RNA processing in human mitochondria. Nature. 1981, 290: 470-474. 10.1038/290470a0.CrossRefPubMed
60.
go back to reference Oliveira MT, Azeredo-Espin AML, Lessinger AC: The mitochondrial DNA control region of Muscidae flies: evolution and structural conservation in a Dipteran context. J Mol Evol. 2007, 64: 519-527. 10.1007/s00239-006-0099-6.CrossRefPubMed Oliveira MT, Azeredo-Espin AML, Lessinger AC: The mitochondrial DNA control region of Muscidae flies: evolution and structural conservation in a Dipteran context. J Mol Evol. 2007, 64: 519-527. 10.1007/s00239-006-0099-6.CrossRefPubMed
61.
62.
63.
go back to reference Caccone A, Garcia BA, Powell JR: Evolution of the mitochondrial DNA control region in the Anopheles gambiae complex. Insect Mol Biol. 1996, 5: 51-59. 10.1111/j.1365-2583.1996.tb00040.x.CrossRefPubMed Caccone A, Garcia BA, Powell JR: Evolution of the mitochondrial DNA control region in the Anopheles gambiae complex. Insect Mol Biol. 1996, 5: 51-59. 10.1111/j.1365-2583.1996.tb00040.x.CrossRefPubMed
64.
go back to reference Duarte GT, De Azeredo-Espin AM, Junqueira AC: The mitochondrial control region of blowflies (Diptera: Calliphoridae): a hot spot for mitochondrial genome rearrangements. J Med Entomol. 2008, 45: 667-76. 10.1603/0022-2585(2008)45[667:TMCROB]2.0.CO;2.CrossRefPubMed Duarte GT, De Azeredo-Espin AM, Junqueira AC: The mitochondrial control region of blowflies (Diptera: Calliphoridae): a hot spot for mitochondrial genome rearrangements. J Med Entomol. 2008, 45: 667-76. 10.1603/0022-2585(2008)45[667:TMCROB]2.0.CO;2.CrossRefPubMed
65.
go back to reference Schultheis AS, Weigt LA, Hendricks AC: Arrangement and structural conservation of the mitochondrial control region of two species of Plecoptera: utility of tandem repeat-containing regions in studies of population genetics and evolutionary history. Insect Mol Biol. 2002, 11: 605-610. 10.1046/j.1365-2583.2002.00371.x.CrossRefPubMed Schultheis AS, Weigt LA, Hendricks AC: Arrangement and structural conservation of the mitochondrial control region of two species of Plecoptera: utility of tandem repeat-containing regions in studies of population genetics and evolutionary history. Insect Mol Biol. 2002, 11: 605-610. 10.1046/j.1365-2583.2002.00371.x.CrossRefPubMed
66.
go back to reference Anisimova M, Bielawski JP, Yang Z: Accuracy and power of Bayes prediction of amino acid sites under positive selection. Mol Biol Evol. 2002, 19: 950-958.CrossRefPubMed Anisimova M, Bielawski JP, Yang Z: Accuracy and power of Bayes prediction of amino acid sites under positive selection. Mol Biol Evol. 2002, 19: 950-958.CrossRefPubMed
67.
go back to reference Anisimova M, Bielawski J, Dunn K, Yang Z: Phylogenomic analysis of natural selection pressure in Streptococcus genomes. BMC Evol Biol. 2007, 7: 154-10.1186/1471-2148-7-154.PubMedCentralCrossRefPubMed Anisimova M, Bielawski J, Dunn K, Yang Z: Phylogenomic analysis of natural selection pressure in Streptococcus genomes. BMC Evol Biol. 2007, 7: 154-10.1186/1471-2148-7-154.PubMedCentralCrossRefPubMed
68.
go back to reference Lehmann T, Hume JC, Licht M, Burns CS, Wollenberg K, Simard F, Ribeiro JM: Molecular evolution of immune genes in the malaria mosquito Anopheles gambiae. PLoS One. 2009, 4: e4549-10.1371/journal.pone.0004549.PubMedCentralCrossRefPubMed Lehmann T, Hume JC, Licht M, Burns CS, Wollenberg K, Simard F, Ribeiro JM: Molecular evolution of immune genes in the malaria mosquito Anopheles gambiae. PLoS One. 2009, 4: e4549-10.1371/journal.pone.0004549.PubMedCentralCrossRefPubMed
69.
go back to reference Edwards FW: Diptera fam. Culicidae. Edited by: Wytsman P. 1932, Genera Insectorum. Desmet- Verteneuil, Brussels Edwards FW: Diptera fam. Culicidae. Edited by: Wytsman P. 1932, Genera Insectorum. Desmet- Verteneuil, Brussels
70.
go back to reference Henning W: Insect phylogeny. 1981, Wiley, Chichester, UK Henning W: Insect phylogeny. 1981, Wiley, Chichester, UK
71.
go back to reference Reidenbach KR, Cook S, Bertone MA, Harbach RE, Wiegmann BM, Besansky NJ: Phylogenetic analysis and temporal diversification of mosquitoes (Diptera: Culicidae) based on nuclear genes and morphology. BMC Evol Biol. 2009, 9: 298-10.1186/1471-2148-9-298.PubMedCentralCrossRefPubMed Reidenbach KR, Cook S, Bertone MA, Harbach RE, Wiegmann BM, Besansky NJ: Phylogenetic analysis and temporal diversification of mosquitoes (Diptera: Culicidae) based on nuclear genes and morphology. BMC Evol Biol. 2009, 9: 298-10.1186/1471-2148-9-298.PubMedCentralCrossRefPubMed
72.
go back to reference Rai KS, Black WC: Mosquito genomes: structure, organization and evolution. Adv Genet. 1999, 41: 1-33. full_text.CrossRefPubMed Rai KS, Black WC: Mosquito genomes: structure, organization and evolution. Adv Genet. 1999, 41: 1-33. full_text.CrossRefPubMed
73.
go back to reference Müller J, Reisz RR: Four well-constrained calibration points from the vertebrate fossil record for molecular clock estimates. Bioessays. 2005, 27: 1069-1075. 10.1002/bies.20286.CrossRefPubMed Müller J, Reisz RR: Four well-constrained calibration points from the vertebrate fossil record for molecular clock estimates. Bioessays. 2005, 27: 1069-1075. 10.1002/bies.20286.CrossRefPubMed
75.
76.
go back to reference Lehmann T, Diabate A: The molecular forms of Anopheles gambiae: a phenotypic perspective. Infect Genet Evol. 2008, 8: 737-746. 10.1016/j.meegid.2008.06.003.PubMedCentralCrossRefPubMed Lehmann T, Diabate A: The molecular forms of Anopheles gambiae: a phenotypic perspective. Infect Genet Evol. 2008, 8: 737-746. 10.1016/j.meegid.2008.06.003.PubMedCentralCrossRefPubMed
77.
78.
go back to reference Turner TL, Hahn MW: Locus- and population-specific selection and differentiation between incipient species of Anopheles gambiae. Mol Biol Evol. 2007, 24: 2132-2138. 10.1093/molbev/msm143.CrossRefPubMed Turner TL, Hahn MW: Locus- and population-specific selection and differentiation between incipient species of Anopheles gambiae. Mol Biol Evol. 2007, 24: 2132-2138. 10.1093/molbev/msm143.CrossRefPubMed
80.
go back to reference Carter R: Speculations on the origins of Plasmodium vivax malaria. Trends Parasitol. 2003, 19: 214-9. 10.1016/S1471-4922(03)00070-9.CrossRefPubMed Carter R: Speculations on the origins of Plasmodium vivax malaria. Trends Parasitol. 2003, 19: 214-9. 10.1016/S1471-4922(03)00070-9.CrossRefPubMed
81.
go back to reference Hume JC, Lyons EJ, Day KP: Human migration, mosquitoes and the evolution of Plasmodium falciparum. Trends Parasitol. 2003, 19: 144-9. 10.1016/S1471-4922(03)00008-4.CrossRefPubMed Hume JC, Lyons EJ, Day KP: Human migration, mosquitoes and the evolution of Plasmodium falciparum. Trends Parasitol. 2003, 19: 144-9. 10.1016/S1471-4922(03)00008-4.CrossRefPubMed
Metadata
Title
Complete mtDNA genomes of Anopheles darlingi and an approach to anopheline divergence time
Authors
Marta Moreno
Osvaldo Marinotti
Jaroslaw Krzywinski
Wanderli P Tadei
Anthony A James
Nicole L Achee
Jan E Conn
Publication date
01-12-2010
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2010
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-9-127

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