Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Advertisement

Heredity
  • View all journals
  • Search
  • Log in
  • Content Explore content
  • About the journal
  • Publish with us
  • Sign up for alerts
  • RSS feed
  1. nature
  2. heredity
  3. original article
  4. article
Structure of rDNA in the mosquito Anopheles gambiae and rDNA sequence variation within and between species of the A. gambiae complex
Download PDF
Download PDF
  • Original Article
  • Published: 01 April 1989

Structure of rDNA in the mosquito Anopheles gambiae and rDNA sequence variation within and between species of the A. gambiae complex

  • Denson Kelly McLain1 nAff2 &
  • Frank H Collins1 

Heredity volume 62, pages 233–242 (1989)Cite this article

  • 2238 Accesses

  • 20 Citations

  • Metrics details

Abstract

The structure of the rDNA repeating unit of Anopheles gambiae (Diptera: Culicidae) was determined by restriction endonuclease mapping and hybridization analyses on four independent clones obtained from a genomic library of a colony (G3) from the Gambia (West Africa). rDNA gene coding sequences are conserved, but much intragenomic and intraspecific (geographic) variation occurs in the intergenic spacer. Hybridization of subclones from spacer and coding sequences to genomic DNA that was isolated from single mosquitoes from laboratory colonies of four other A. gambiae complex species reveals conservation of coding sequences but concerted evolution in the intergenic spacers.

Similar content being viewed by others

High-throughput barcoding method for the genetic surveillance of insecticide resistance and species identification in Anopheles gambiae complex malaria vectors

Article Open access 16 August 2022

Deep learning and wing interferential patterns identify Anopheles species and discriminate amongst Gambiae complex species

Article Open access 25 August 2023

Anopheles gambiae on remote islands in the Indian Ocean: origins and prospects for malaria elimination by genetic modification of extant populations

Article Open access 27 November 2023

Article PDF

References

  • Amstutz, H, Munz, P, Heyer, W D, Leupold, U, and Kohli, J. 1985. Concerted evolution of transfer RNA genes: intergenic conversion among three unlinked serine transfer RNA genes in Schizosaccharomyces pombe. Cell, 40, 879–886.

    Article  CAS  PubMed  Google Scholar 

  • Arnheim, N. 1983. concerted evolution of multigene families. In Nei, M. and Koehn, R. K. (ed.) Evolution of Genes and Proteins, Sinauer, Boston, pp. 38–61.

    Google Scholar 

  • Beckingham, K. 1982. Insect rDNA. Cell NucL, 10, 205–263.

    CAS  Google Scholar 

  • Beckingham, K, and Smith, V L. 1981. The ribosomal DNA of Calliphora erythrocephala: the cistron classes of total genomic DNA. J Mol Biol, 149, 141–169.

    Article  CAS  PubMed  Google Scholar 

  • Beckingham, K, and White, R. 1980. The ribosomal DNA of Calliphora erythrocephala: an analysis of hybrid plas-mids containing ribosomal DNA. J Mol Biol, 137, 349–373.

    Article  CAS  PubMed  Google Scholar 

  • Boncinelli, E, Borhese, A, Graziani, F, Lamantia, A, Manzi, A, Mriani, C, and Simeone, A. 1983. Inheritance of the rDNA spacer in Drosophila. Mol Gen Genet, 189, 370–374.

    Article  CAS  Google Scholar 

  • Coen, E S, and Dover, G A. 1982. Multiple Pol I intiation sites in rDNA spacers of Drosophila melanogaster. Nucl Acids Res, 10, 7017–7026.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coen, E S, and Dover, G A. 1983. Unequal exchanges and the coevolution of X and Y chromosomal rDNA arrays in Drosophila melanogaster. Cell 33, 849–854.

    Article  CAS  PubMed  Google Scholar 

  • Coen, E, Strachan, T, and Dover, G A. 1982a. Dynamics of concerted evolution of ribosomal DNA and histone gene families in the melanogaster subgroup of Drosophila. J Mol Biol, 158, 17–35.

    Article  CAS  PubMed  Google Scholar 

  • Coen, E S, Thoday, J M, and Dover, G A. 1982b. The rate of turnover of structural variants in the ribosomal gene family of Drosophila melanogaster. Nature, 295, 564–568.

    Article  CAS  PubMed  Google Scholar 

  • Collins, F H, Mendez, A, Rassmusen, M O, Mehaffey, P C, Besansky, N J, and Finnerty, V. 1987. A ribo-somal RNA gene probe differentiates member species of the Anopheles gambiae complex. Am J Trop Med Hyg, 37, 37–41.

    Article  CAS  PubMed  Google Scholar 

  • Desalle, R, Slightorn, J, and Zimmer, E. 1986. The molecular through ecological genetics of abnormal abdomen. II. Ribosomal DNA polymorphism is associated with the abnormal abdomen syndrome in Drosophila mer-catorum. Genetics, 112, 861–875.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dewinter, R F J, and Moss, T. 1986. Spacer promoters are essential for efficient enhancement of X. laevis ribosomal transcription. Cell, 44, 313–318.

    Article  CAS  Google Scholar 

  • Dover, G A. 1982. Molecular drive: a cohesive mode of species evolution. Nature, 299, 111–117.

    Article  CAS  PubMed  Google Scholar 

  • Dover, G A. 1986. Molecular drive in multigene families: how biological novelties arise, spread and are assimilated. Trends Genet, 2, 159–165.

    Article  CAS  Google Scholar 

  • Dover, G A, Brown, S, Coen, E S, Dallas, J, Strachan, T, and Trick, M. 1982. The dynamics of genome evolution and species differentiation. In Dover, G. A. and Flavell, R. B. (ed.) Genome, Evolution, Academic Press, New York, pp. 343–372.

    Google Scholar 

  • Dover, G A, and Coen, E. 1981. Spring cleaning ribosomal DNA: a model for multigene evolution? Nature, 290, 731–732.

    Article  CAS  PubMed  Google Scholar 

  • Dover, G A, and Flavell, R B. 1984. Molecular coevolution: DNA divergence and the maintenance of function. Cell, 38, 622–623.

    Article  CAS  PubMed  Google Scholar 

  • Dutton, F L, and Krider, H M. 1984. Ribosomal RNA cistrons of X-chromosomes clonally derived from Drosophila melanogaster laboratory populations: redundancy, organization and stability. Genetics, 107, 405–421.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Endow, S A, and Glover, D M. 1979. Differential replication of ribosomal gene repeats in polytene nuclei of Drosophila. Cell, 17, 597–605.

    Article  CAS  PubMed  Google Scholar 

  • Erickson, J M, and Schmickell, R D. 1985. A molecular basis for discrete variation in human ribosomal DNA. Am J Hum Genet, 37, 311–325.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Federoff, N V. 1979. On spacers. Cell, 16, 697–710.

    Article  Google Scholar 

  • Gerbi, S A. 1985. Evolution of ribosomal DNA. In Maclntyre, R. (ed.) Molecular Evolutionary Genetics, Plenum, New York, pp. 419–517.

    Chapter  Google Scholar 

  • Gillings, M R, Frankham, R, Spiers, J, and Whalley, M. 1987. X-Y exchange and the coevolution of the X and Y rDNA arrays in Drosophila melanogaster. Genetics, 116, 241–251.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hayashida, H, Miyata, T, Ymawaki-Katooka, Y, Honjo, T, Wels, J, and Blattner, F. 1984. Concerted evolution of the mouse immunoglobulin gamma chain genes. EMBO J, 3, 2047–2054.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jubier-Maurin, V, Dod, B J, Bellis, M, Piechaczyk, M, and Roizes, G. 1985. Comparative study of the LI family in the genus Mu: possible role of retroposition and conversion events in its concerted evolution. J Mol Biol, 184, 547–564.

    Article  CAS  PubMed  Google Scholar 

  • Kalamuck, K E, and Procunier, J D. 1984. Non-selective amplification of ribosomal DNA repeat units in compensating genotypes of Drosophila melanogaster. Biochem Genet, 22, 453–465.

    Article  Google Scholar 

  • Keil, R L, and Roeder, G S. 1984. Cis-acting, recombination-stimulating activity in a fragment of the ribosomal DNA of Saccharomyces cerevisiae. Cell, 39, 377–386.

    Article  CAS  PubMed  Google Scholar 

  • Kidd, S J, and Glover, D M. 1980. A DNA segment from Drosophila melanogaster which contains five tandemly repeating units homologous to the major rDNA insertion. Cell, 19, 103–119.

    Article  CAS  PubMed  Google Scholar 

  • Kohorn, B D, and Rae, P M M. 1982. Non-transcribed spacer sequences promote in vitro transcription of Drosophila melanogaster ribosomal DNA. Nucl Acids Res, 10, 6879–6886.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kunz, W, Petersen, G, Renkawitz-Pohl, R, Glatzer, K H, and Schafer, M. 1981. Distribution of spacer length classes and the intervening sequence among different nucleolus organizers in Drosophila hydei. Chromosoma, 83, 145–158.

    Article  CAS  PubMed  Google Scholar 

  • Livak, K. 1984. Organization and mapping of a sequence on the Drosophila melanogaster X and Y chromosomes that is transcribed during spermatogenesis. Genetics, 107, 611–634.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Long, E O, Collins, M, Kiefer, B I, and Dawid, I B. 1981. Expression of the ribosomal DNA insertions in bobbed mutants of Drosophila melanogaster. Mol Gen Genet, 182, 377–384.

    Article  CAS  PubMed  Google Scholar 

  • Maddern, R H. 1981. Exchange between ribosomal RNA genes of the X and Y chromosomes of Drosophila melanogaster. Genet Res, 38, 1–7.

    Article  CAS  PubMed  Google Scholar 

  • Maniatis, T, Fritsch, E F, and Sambrook, J. 1982. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory.

    Google Scholar 

  • Mendez, A M, Collins, F H, and Finnerty, V. 1988. Organization of the 28S gene intron of rDNA in Anopheles gambiae. (Manuscript in preparation).

  • Michelson, A M, and Orkin, S H. 1983. Boundaries of gene conversion within the duplicated human a-globin genes: concerted evolution by segmental recombination. J Biol Chem, 258, 15245–15254.

    CAS  PubMed  Google Scholar 

  • Morzycka-Wroblewska, E, Selker, E U, Stevens, J N, and Metzenberg, R L. 1985. Concerted evolution of dispersed Neurospora crassa 58 RNA genes: pattern of sequence conservation between allelic and nonallelic genes. Mol Cell Biol, 5, 46–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohta, T. 1983. On the evolution of multigene families. Theor Pop Biol, 23, 216–240.

    Article  CAS  Google Scholar 

  • Ohta, T, and Dover, G A. 1983. Population genetics of multigene families that are dispersed into two or more chromosomes. Proc Natl Acad Sci (USA), 80, 4079–4083.

    Article  CAS  Google Scholar 

  • Ohta, T, and Dover, G A. 1984. The cohesive population genetics of molecular drive. Genetics, 108, 501–521.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Peacock, W J, Appels, R, Endow, S, and Glover, D M. 1981. Chromosomal distribution of the major insert in Drosophila melanogaster 28S rRNA genes. Genet Res, 37, 204–214.

    Article  Google Scholar 

  • Pichersky, E, Bernatzky, R, Tanksley, S D, and Cashmore, A R. 1986. Evidence for selection as a mechanism in the concerted evolution of Lycopersicon esculentum (tomato) genes encoding the small subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase. Proc Natl Acad Sci (USA), 83, 3880–3884.

    Article  CAS  Google Scholar 

  • Reeder, R J. 1984. Enhancers and ribosomal gene spacers. Cell, 38, 349–351.

    Article  CAS  PubMed  Google Scholar 

  • Roiha, H, and Glover, D M. 1980. Characterization of complete type II insertions in cloned segments of ribosomal DNA from Drosophila melanogaster. J Mol Biol, 140, 341–355.

    Article  CAS  PubMed  Google Scholar 

  • Roiha, H, Miller, J R, Woods, L C, and Glover, D M. 1981. Arrangements and rearrangements of sequence flanking the two types of rDNA insertion in Drosophila melanogaster. Nature, 290, 749–753.

    Article  CAS  PubMed  Google Scholar 

  • Roiha, H, Read, C A, Browne, M J, and Glover, D M. 1983. Widely differing degrees of sequence conservation of the two types of rDNA insertion within the melanogaster species subgroup of Drosophila. EMBO J, 2, 721–726.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salzano, G, and Malva, C. 1984. Non-random loss of uninterrupted ribosomal DNA repeating units upon induction of a bobbed mutation. J Mol Biol, 177, 189–200.

    Article  CAS  PubMed  Google Scholar 

  • Schimenti, J C, and Duncan, C H. 1985. Concerted evolution of the cow beta-globin genes. Mol Biol Evol, 2, 505–513.

    CAS  PubMed  Google Scholar 

  • Service, M W. 1985. Anopheles gambiae: Africa's principal malaria vector, 1902–1984 Bull Entomol Soc Am, Fall, 8–12.

    Article  Google Scholar 

  • Southern, E. 1975. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol, 98, 503–517.

    Article  CAS  PubMed  Google Scholar 

  • Strachan, T, Coen, E, Webb, D, and Dover, G A. 1982. Modes and rates of change of complex DNA families of Drosophila. J Mol Biol, 158, 37–54.

    Article  CAS  PubMed  Google Scholar 

  • Strachan, T, Webb, D, and Dover, G A. 1985. Transition stages of molecular drive in multi-copy DNA families in Drosophila. EMBO J, 4, 1701–1708.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tautz, D, and Dover, G A. 1986. Transcription of the tandem array of ribosomal DNA of Drosophila melanogaster does not terminate at any fixed point. EMBO J, 5, 1267–1273.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tautz, D, Tautz, C, Webb, D, and Dover, G A. 1987. Evolutionary divergence of promoters and spacers in the rDNA family of four Drosophila species. J Mol Biol, 195, 425–542.

    Article  Google Scholar 

  • Tautz, D, Trick, M, and Dover, G A. 1986. Cryptic simplicity in DNA is a major source of genetic variation. Nature, 322, 652–656.

    Article  CAS  PubMed  Google Scholar 

  • Treco, D, Brownell, E, and Arnheim, N. 1982. The ribosomal gene nontranscribed spacer. Cell Nucl, 12, 101–126.

    CAS  Google Scholar 

  • Vieira, J, and Messing, J. 1982. The pUC plasmids, an Mal3mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene, 19, 259–268.

    Article  CAS  PubMed  Google Scholar 

  • Williams, S M, Desalle, R, and Strobeck, C. 1985. Homogenization of geographical variants at the nontranscribed spacer of rDNA in Drosophila mercatorum. Mol Biol Evol, 2, 338–346.

    CAS  PubMed  Google Scholar 

  • Williams, S M, Furnier, G R, Fuog, E, and Strobeck, C. 1987. Evolution of ribosomal DNA spacers of Drosophila melanogaster: different patterns of variation on X and Y chromosomes. Genetics, 116, 225–232.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Williams, S M, and Strobeck, C. 1985. Sister chromatid exchange and the evolution of rDNA length. J Theor Biol 116, 625–636.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Author notes
  1. Denson Kelly McLain

    Present address: Department of Biology, Georgia Southern College, Statesboro, GA, 30460, U.S.A.

Authors and Affiliations

  1. Division of Parastitic Diseases, Malaria Branch, Center for Infection Diseases, Centers for Disease Control, Atlanta, 30333, GA, USA

    Denson Kelly McLain & Frank H Collins

Authors
  1. Denson Kelly McLain
    View author publications

    Search author on:PubMed Google Scholar

  2. Frank H Collins
    View author publications

    Search author on:PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

McLain, D., Collins, F. Structure of rDNA in the mosquito Anopheles gambiae and rDNA sequence variation within and between species of the A. gambiae complex. Heredity 62, 233–242 (1989). https://doi.org/10.1038/hdy.1989.33

Download citation

  • Received: 01 August 1988

  • Issue date: 01 April 1989

  • DOI: https://doi.org/10.1038/hdy.1989.33

Share this article

Anyone you share the following link with will be able to read this content:

Sorry, a shareable link is not currently available for this article.

Provided by the Springer Nature SharedIt content-sharing initiative

This article is cited by

  • Is higher-order structure conserved in eukaryotic ribosomal DNA intergenic spacers?

    • Gerald D. Baldridge
    • Mark Wm. Dalton
    • Ann M. Fallon

    Journal of Molecular Evolution (1992)

  • Microgeographic variation in rDNA intergenic spacers of Anopheles gambiae in western Kenya

    • Denson Kelly McLain
    • Frank H Collins
    • J B O Were

    Heredity (1989)

Download PDF

Advertisement

Explore content

  • Research articles
  • Reviews & Analysis
  • News & Comment
  • Podcasts
  • Current issue
  • Collections
  • Follow us on Twitter
  • Sign up for alerts
  • RSS feed

About the journal

  • Journal Information
  • Open access publishing
  • About the Editors
  • Contact
  • About the Partner
  • For Advertisers
  • Subscribe

Publish with us

  • For Authors & Referees
  • Language editing services
  • Open access funding
  • Submit manuscript

Search

Advanced search

Quick links

  • Explore articles by subject
  • Find a job
  • Guide to authors
  • Editorial policies

Heredity (Heredity)

ISSN 1365-2540 (online)

ISSN 0018-067X (print)

nature.com sitemap

About Nature Portfolio

  • About us
  • Press releases
  • Press office
  • Contact us

Discover content

  • Journals A-Z
  • Articles by subject
  • protocols.io
  • Nature Index

Publishing policies

  • Nature portfolio policies
  • Open access

Author & Researcher services

  • Reprints & permissions
  • Research data
  • Language editing
  • Scientific editing
  • Nature Masterclasses
  • Research Solutions

Libraries & institutions

  • Librarian service & tools
  • Librarian portal
  • Open research
  • Recommend to library

Advertising & partnerships

  • Advertising
  • Partnerships & Services
  • Media kits
  • Branded content

Professional development

  • Nature Awards
  • Nature Careers
  • Nature Conferences

Regional websites

  • Nature Africa
  • Nature China
  • Nature India
  • Nature Japan
  • Nature Middle East
  • Privacy Policy
  • Use of cookies
  • Legal notice
  • Accessibility statement
  • Terms & Conditions
  • Your US state privacy rights
Springer Nature

© 2025 Springer Nature Limited