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. 1998 Oct;150(2):807–814. doi: 10.1093/genetics/150.2.807

Multiple origins of cytologically identical chromosome inversions in the Anopheles gambiae complex.

A Caccone 1, G S Min 1, J R Powell 1
PMCID: PMC1460344  PMID: 9755210

Abstract

For more than 60 years, evolutionary cytogeneticists have been using naturally occurring chromosomal inversions to infer phylogenetic histories, especially in insects with polytene chromosomes. The validity of this method is predicated on the assumption that inversions arise only once in the history of a lineage, so that sharing a particular inversion implies shared common ancestry. This assumption of monophyly has been generally validated by independent data. We present the first clear evidence that naturally occurring inversions, identical at the level of light microscopic examination of polytene chromosomes, may not always be monophyletic. The evidence comes from DNA sequence analyses of regions within or very near the breakpoints of an inversion called the 2La that is found in the Anopheles gambiae complex. Two species, A. merus and A. arabiensis, which are fixed for the "same" inversion, do not cluster with each other in a phylogenetic analysis of the DNA sequences within the 2La. Rather, A. merus 2La is most closely related to strains of A. gambiae homozygous for the 2L+. A. gambiae and A. merus are sister taxa, the immediate ancestor was evidently homozygous 2L+, and A. merus became fixed for an inversion cytologically identical to that in A. arabiensis. A. gambiae is polymorphic for 2La/2L+, and the 2La in this species is nearly identical at the DNA level to that in A. arabiensis, consistent with the growing evidence that introgression has or is occurring between these two most important vectors of malaria in the world. The parallel evolution of the "same" inversion may be promoted by the presence of selectively important genes within the breakpoints.

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Selected References

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  1. 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]
  2. 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]
  3. Coluzzi M., Sabatini A., Petrarca V., Di Deco M. A. Behavioural divergences between mosquitoes with different inversion karyotypes in polymorphic populations of the Anopheles gambiae complex. Nature. 1977 Apr 28;266(5605):832–833. doi: 10.1038/266832a0. [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. García B. A., Caccone A., Mathiopoulos K. D., Powell J. R. Inversion monophyly in African anopheline malaria vectors. Genetics. 1996 Jul;143(3):1313–1320. doi: 10.1093/genetics/143.3.1313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Kishino H., Hasegawa M. Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in hominoidea. J Mol Evol. 1989 Aug;29(2):170–179. doi: 10.1007/BF02100115. [DOI] [PubMed] [Google Scholar]
  8. Larson A. The comparison of morphological and molecular data in phylogenetic systematics. EXS. 1994;69:371–390. doi: 10.1007/978-3-0348-7527-1_22. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. 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]
  11. Petrarca V., Beier J. C. Intraspecific chromosomal polymorphism in the Anopheles gambiae complex as a factor affecting malaria transmission in the Kisumu area of Kenya. Am J Trop Med Hyg. 1992 Feb;46(2):229–237. doi: 10.4269/ajtmh.1992.46.229. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Popadić A., Popadić D., Anderson W. W. Interchromosomal exchange of genetic information between gene arrangements on the third chromosome of Drosophila pseudoobscura. Mol Biol Evol. 1995 Sep;12(5):938–943. doi: 10.1093/oxfordjournals.molbev.a040271. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. 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]
  16. 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]
  17. Tamura K., Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol. 1993 May;10(3):512–526. doi: 10.1093/oxfordjournals.molbev.a040023. [DOI] [PubMed] [Google Scholar]
  18. Vernick K. D., Collins F. H., Gwadz R. W. A general system of resistance to malaria infection in Anopheles gambiae controlled by two main genetic loci. Am J Trop Med Hyg. 1989 Jun;40(6):585–592. doi: 10.4269/ajtmh.1989.40.585. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. della Torre A., Favia G., Mariotti G., Coluzzi M., Mathiopoulos K. D. Physical map of the malaria vector Anopheles gambiae. Genetics. 1996 Jul;143(3):1307–1311. doi: 10.1093/genetics/143.3.1307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. della Torre A., Merzagora L., Powell J. R., Coluzzi M. Selective introgression of paracentric inversions between two sibling species of the Anopheles gambiae complex. Genetics. 1997 May;146(1):239–244. doi: 10.1093/genetics/146.1.239. [DOI] [PMC free article] [PubMed] [Google Scholar]

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