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. 1996 Jul;143(3):1313–1320. doi: 10.1093/genetics/143.3.1313

Inversion Monophyly in African Anopheline Malaria Vectors

B A Garcia 1, A Caccone 1, K D Mathiopoulos 1, J R Powell 1
PMCID: PMC1207400  PMID: 8807303

Abstract

The African Anopheles gambiae complex of six sibling species has many polymorphic and fixed paracentric inversions detectable in polytene chromosomes. These have been used to infer phylogenetic relationships as classically done with Drosophila. Two species, A. gambiae and A. merus, were thought to be sister taxa based on a shared X inversion designated X(ag). Recent DNA data have conflicted with this phylogenetic inference as they have supported a sister taxa relationship of A. gambiae and A. arabiensis. A possible explanation is that the X(ag) is not monophyletic. Here we present data from a gene (soluble guanylate cyclase) within the X(ag) that strongly supports the monophyly of the X(ag). We conjecture that introgression may be occurring between the widely sympatric species A. gambiae and A. arabiensis and that the previous DNA phylogenies have been detecting the introgression. Evidently, introgression is not uniform across the genome, and species-specific regions, like the X-chromosome inversions, do not introgress probably due to selective elimination in hybrids and backcrosses.

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Selected References

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  1. Aquadro C. F., Weaver A. L., Schaeffer S. W., Anderson W. W. Molecular evolution of inversions in Drosophila pseudoobscura: the amylase gene region. Proc Natl Acad Sci U S A. 1991 Jan 1;88(1):305–309. doi: 10.1073/pnas.88.1.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Besansky N. J., Powell J. R., Caccone A., Hamm D. M., Scott J. A., Collins F. H. Molecular phylogeny of the Anopheles gambiae complex suggests genetic introgression between principal malaria vectors. Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):6885–6888. doi: 10.1073/pnas.91.15.6885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Caccone A., Garcia B. A., Powell J. R. Evolution of the mitochondrial DNA control region in the Anopheles gambiae complex. Insect Mol Biol. 1996 Feb;5(1):51–59. doi: 10.1111/j.1365-2583.1996.tb00040.x. [DOI] [PubMed] [Google Scholar]
  4. Coluzzi M., Sabatini A., Petrarca V., Di Deco M. A. Chromosomal differentiation and adaptation to human environments in the Anopheles gambiae complex. Trans R Soc Trop Med Hyg. 1979;73(5):483–497. doi: 10.1016/0035-9203(79)90036-1. [DOI] [PubMed] [Google Scholar]
  5. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol. 1981;17(6):368–376. doi: 10.1007/BF01734359. [DOI] [PubMed] [Google Scholar]
  6. Ferris S. D., Sage R. D., Huang C. M., Nielsen J. T., Ritte U., Wilson A. C. Flow of mitochondrial DNA across a species boundary. Proc Natl Acad Sci U S A. 1983 Apr;80(8):2290–2294. doi: 10.1073/pnas.80.8.2290. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gatti M., Santini G., Pimpinelli S., Coluzz M. Fluorescence banding techniques in the identification of sibling species of the anopheles gambiae complex. Heredity (Edinb) 1977 Feb;38(1):105–108. doi: 10.1038/hdy.1977.11. [DOI] [PubMed] [Google Scholar]
  8. Giuili G., Scholl U., Bulle F., Guellaën G. Molecular cloning of the cDNAs coding for the two subunits of soluble guanylyl cyclase from human brain. FEBS Lett. 1992 Jun 8;304(1):83–88. doi: 10.1016/0014-5793(92)80594-7. [DOI] [PubMed] [Google Scholar]
  9. Gojobori T., Ishii K., Nei M. Estimation of average number of nucleotide substitutions when the rate of substitution varies with nucleotide. J Mol Evol. 1982;18(6):414–423. doi: 10.1007/BF01840889. [DOI] [PubMed] [Google Scholar]
  10. Gyllensten U. B., Erlich H. A. Generation of single-stranded DNA by the polymerase chain reaction and its application to direct sequencing of the HLA-DQA locus. Proc Natl Acad Sci U S A. 1988 Oct;85(20):7652–7656. doi: 10.1073/pnas.85.20.7652. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Livak K. J. Organization and mapping of a sequence on the Drosophila melanogaster X and Y chromosomes that is transcribed during spermatogenesis. Genetics. 1984 Aug;107(4):611–634. doi: 10.1093/genetics/107.4.611. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Mathiopoulos K. D., Lanzaro G. C. Distribution of genetic diversity in relation to chromosomal inversions in the malaria mosquito Anopheles gambiae. J Mol Evol. 1995 Jun;40(6):578–584. doi: 10.1007/BF00160504. [DOI] [PubMed] [Google Scholar]
  13. Mathiopoulos K. D., Powell J. D., McCutchan T. F. An anchored restriction-mapping approach applied to the genetic analysis of the Anopheles gambiae malaria vector complex 1. Mol Biol Evol. 1995 Jan;12(1):103–112. doi: 10.1093/oxfordjournals.molbev.a040179. [DOI] [PubMed] [Google Scholar]
  14. Petrarca V., Beier J. C., Onyango F., Koros J., Asiago C., Koech D. K., Roberts C. R. Species composition of the Anopheles gambiae complex (diptera: Culicidae) at two sites in western Kenya. J Med Entomol. 1991 May;28(3):307–313. doi: 10.1093/jmedent/28.3.307. [DOI] [PubMed] [Google Scholar]
  15. Popadić A., Anderson W. W. The history of a genetic system. Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):6819–6823. doi: 10.1073/pnas.91.15.6819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Rozas J., Aguadé M. Gene conversion is involved in the transfer of genetic information between naturally occurring inversions of Drosophila. Proc Natl Acad Sci U S A. 1994 Nov 22;91(24):11517–11521. doi: 10.1073/pnas.91.24.11517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  18. Shah S., Hyde D. R. Two Drosophila genes that encode the alph and beta subunits of the brain soluble guanylyl cyclase. J Biol Chem. 1995 Jun 23;270(25):15368–15376. doi: 10.1074/jbc.270.25.15368. [DOI] [PubMed] [Google Scholar]
  19. Sturtevant A. H., Dobzhansky T. Inversions in the Third Chromosome of Wild Races of Drosophila Pseudoobscura, and Their Use in the Study of the History of the Species. Proc Natl Acad Sci U S A. 1936 Jul;22(7):448–450. doi: 10.1073/pnas.22.7.448. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Tajima F., Nei M. Estimation of evolutionary distance between nucleotide sequences. Mol Biol Evol. 1984 Apr;1(3):269–285. doi: 10.1093/oxfordjournals.molbev.a040317. [DOI] [PubMed] [Google Scholar]
  21. Takahata N., Kimura M. A model of evolutionary base substitutions and its application with special reference to rapid change of pseudogenes. Genetics. 1981 Jul;98(3):641–657. doi: 10.1093/genetics/98.3.641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Wesley C. S., Eanes W. F. Isolation and analysis of the breakpoint sequences of chromosome inversion In(3L)Payne in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1994 Apr 12;91(8):3132–3136. doi: 10.1073/pnas.91.8.3132. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. White G. B. Anopheles gambiae complex and disease transmission in Africa. Trans R Soc Trop Med Hyg. 1974;68(4):278–301. doi: 10.1016/0035-9203(74)90035-2. [DOI] [PubMed] [Google Scholar]
  24. White G. B. Chromosomal evidence for natural interspecific hybridization by mosquitoes of the Anopheles gambiae complex. Nature. 1971 May 21;231(5299):184–185. doi: 10.1038/231184a0. [DOI] [PubMed] [Google Scholar]

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