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PMID: 12947038 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Semipermeable species boundaries between Anopheles gambiae and Anopheles arabiensis: evidence from multilocus DNA sequence variation.

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 100 ·No. 19 ·2003-09-16 ·Pages 10818-23

Besansky NJ, Krzywinski J, Lehmann T, Simard F, Kern M, Mukabayire O, Fontenille D, Touré Y, Sagnon N

Abstract

Attempts to reconstruct the phylogenetic history of the Anopheles gambiae cryptic species complex have yielded strongly conflicting results. In particular, An. gambiae, the primary African malaria vector, is variously placed as a sister taxon to either Anopheles arabiensis or Anopheles merus. The recent divergence times for members of this complex complicate phylogenetic analysis, making it difficult to unambiguously implicate interspecific gene flow, versus retained ancestral polymorphism, as the source of conflict. Using sequences at four unlinked loci, which were determined from multiple specimens within each of five species in the complex, we found contrasting patterns of sequence divergence between the X chromosome and the autosomes. The isolation model of speciation assumes a lack of gene flow between species since their separation. This model could not be rejected for An. gambiae and An. arabiensis, although the data fit the model poorly. On the other hand, evidence from gene trees supports genetic introgression of chromosome 2 inversions between An. gambiae and An. arabiensis, and also points to more broad scale genetic exchange of autosomal sequences between this species pair. That such exchange has been relatively recent is suggested not only by the lack of fixed differences at three autosomal loci but also by the sharing of full haplotypes at two of the three loci, which is in contrast to several fixed differences and considerably deeper divergence on the X. The proposed acquisition by An. gambiae of sequences from the more arid-adapted An. arabiensis may have contributed to the spread and ecological dominance of this malaria vector.

MeSH Terms
Animals Anopheles/classification,genetics DNA/genetics Molecular Sequence Data Phylogeny Polymorphism, Genetic Sequence Analysis, DNA Species Specificity
Chemicals
DNA
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Besansky N J
University of Notre Dame, Center for Tropical Disease Research and Training, Department of Biological Sciences, Notre Dame, IN 46556, USA. besansky.1@nd.edu
Krzywinski J
Lehmann T
Simard F
Kern M
Mukabayire O
Fontenille D
Touré Y
Sagnon N'F
References (27)
27 references, click to expand
  1. The distribution and inversion polymorphism of chromosomally recognized taxa of the Anopheles gambiae complex in Mali, West Africa.
    Parassitologia. 1998 Dec;40(4):477-511 PMID: 10645562
  2. Detection of hybrids in natural populations of the Anopheles gambiae complex by the rDNA-based, PCR method.
    Ann Trop Med Parasitol. 1997 Dec;91(8):963-5 PMID: 9579219
  3. The population genetics of the origin and divergence of the Drosophila simulans complex species.
    Genetics. 2000 Dec;156(4):1913-31 PMID: 11102384
  4. Patterns of DNA sequence variation in chromosomally recognized taxa of Anopheles gambiae: evidence from rDNA and single-copy loci.
    Insect Mol Biol. 2001 Feb;10(1):33-46 PMID: 11240635
  5. Genetic population structure and introgression in Anopheles dirus mosquitoes in South-east Asia.
    Mol Ecol. 2001 Mar;10(3):569-80 PMID: 11298969
  6. Evidence for recent population expansion in the evolutionary history of the malaria vectors Anopheles arabiensis and Anopheles gambiae.
    Mol Biol Evol. 2001 Jul;18(7):1353-64 PMID: 11420373
  7. Inferring the history of speciation from multilocus DNA sequence data: the case of Drosophila pseudoobscura and close relatives.
    Mol Biol Evol. 2002 Apr;19(4):472-88 PMID: 11919289
  8. Multiple origins of cytologically identical chromosome inversions in the Anopheles gambiae complex.
    Genetics. 1998 Oct;150(2):807-14 PMID: 9755210
  9. The Anopheles gambiae complex: a new species from Ethiopia.
    Trans R Soc Trop Med Hyg. 1998 Mar-Apr;92(2):231-5 PMID: 9764342
  10. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis.
    Bioinformatics. 1999 Feb;15(2):174-5 PMID: 10089204
  11. Analysis of genetic variability in Anopheles arabiensis and Anopheles gambiae using microsatellite loci.
    Insect Mol Biol. 1999 May;8(2):287-97 PMID: 10380112
  12. Toward understanding Anophelinae (Diptera, Culicidae) phylogeny: insights from nuclear single-copy genes and the weight of evidence.
    Syst Biol. 2001 Aug;50(4):540-56 PMID: 12116652
  13. Chromosomal differentiation and adaptation to human environments in the Anopheles gambiae complex.
    Trans R Soc Trop Med Hyg. 1979;73(5):483-97 PMID: 394408
  14. A test of neutral molecular evolution based on nucleotide data.
    Genetics. 1987 May;116(1):153-9 PMID: 3110004
  15. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism.
    Genetics. 1989 Nov;123(3):585-95 PMID: 2513255
  16. Identification of single specimens of the Anopheles gambiae complex by the polymerase chain reaction.
    Am J Trop Med Hyg. 1993 Oct;49(4):520-9 PMID: 8214283
  17. 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):6885-8 PMID: 8041714
  18. Evolution of the mitochondrial DNA control region in the Anopheles gambiae complex.
    Insect Mol Biol. 1996 Feb;5(1):51-9 PMID: 8630535
  19. Genetic differentiation of Anopheles gambiae populations from East and west Africa: comparison of microsatellite and allozyme loci.
    Heredity (Edinb). 1996 Aug;77 ( Pt 2):192-200 PMID: 8760401
  20. Inversion monophyly in African anopheline malaria vectors.
    Genetics. 1996 Jul;143(3):1313-20 PMID: 8807303
  21. A coalescent estimator of the population recombination rate.
    Genetics. 1997 Mar;145(3):833-46 PMID: 9055092
  22. Estimating ancestral population parameters.
    Genetics. 1997 Mar;145(3):847-55 PMID: 9055093
  23. Selective introgression of paracentric inversions between two sibling species of the Anopheles gambiae complex.
    Genetics. 1997 May;146(1):239-44 PMID: 9136013
  24. Neutral behavior of shared polymorphism.
    Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7730-4 PMID: 9223256
  25. Gene flow and natural selection in the origin of Drosophila pseudoobscura and close relatives.
    Genetics. 1997 Nov;147(3):1091-106 PMID: 9383055
  26. Patterns of mitochondrial variation within and between African malaria vectors, Anopheles gambiae and An. arabiensis, suggest extensive gene flow.
    Genetics. 1997 Dec;147(4):1817-28 PMID: 9409838
  27. Population structure, speciation, and introgression in the Anopheles gambiae complex.
    Parassitologia. 1999 Sep;41(1-3):101-13 PMID: 10697841
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
DOI
10.1073/pnas.1434337100
Email
besansky.1@nd.edu
Published
2003-09-16
Epub
2003-00-28
Pages
10818-23
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC196886
Subset
IM
Grants
NIAID NIH HHS · R01 AI44003 · United States
Databases
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PubMed source DOI: 10.1073/pnas.1434337100 PMC Full Text View journal details
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