Abstract
Preliminary studies with restriction fragment length polymorphisms of mitochondrial DNA (mtDNA) in natural populations of Drosophila melanogaster revealed considerable variation in terms of nucleotide sequence and overall size. In this report we present data from more isofemale lines and more restriction enzymes, and explore the utility of the data in inferring a colonization history of this species. Size variation in the noncoding A + T-rich region is particularly plentiful, with size variants occurring in all restriction site haplotypes in all populations. We report here classes of small-scale mobility polymorphisms (apparent range of 20 bp) in specific restriction fragments in the coding region. The variation in one such fragment appears to be generated even more rapidly than in the noncoding region. On the basis of the distribution of restriction site haplotypes, the species range can be divided into three major regions along longitudinal lines: Euro-African populations are the most diverse and are taken to be oldest; Far East populations have a complex distribution of haplotypes; Western Hemisphere populations are the least diverse and are interpreted to be the youngest. The history inferred from mtDNA alone is remarkably similar to one based on several nuclear markers. The mtDNA haplotype distribution is also very different from that of allozymes in these same populations. We interpret this as further evidence that natural selection is still the most parsimonious explanation for the parallel latitudinal allozyme clines in this species.
Full Text
The Full Text of this article is available as a PDF (3.2 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bermingham E., Lamb T., Avise J. C. Size polymorphism and heteroplasmy in the mitochondrial DNA of lower vertebrates. J Hered. 1986 Jul-Aug;77(4):249–252. doi: 10.1093/oxfordjournals.jhered.a110230. [DOI] [PubMed] [Google Scholar]
- Brown G. G., Simpson M. V. Novel features of animal mtDNA evolution as shown by sequences of two rat cytochrome oxidase subunit II genes. Proc Natl Acad Sci U S A. 1982 May;79(10):3246–3250. doi: 10.1073/pnas.79.10.3246. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cann R. L., Stoneking M., Wilson A. C. Mitochondrial DNA and human evolution. Nature. 1987 Jan 1;325(6099):31–36. doi: 10.1038/325031a0. [DOI] [PubMed] [Google Scholar]
- Carr S. M., Ballinger S. W., Derr J. N., Blankenship L. H., Bickham J. W. Mitochondrial DNA analysis of hybridization between sympatric white-tailed deer and mule deer in west Texas. Proc Natl Acad Sci U S A. 1986 Dec;83(24):9576–9580. doi: 10.1073/pnas.83.24.9576. [DOI] [PMC free article] [PubMed] [Google Scholar]
- David J. R., Capy P. Genetic variation of Drosophila melanogaster natural populations. Trends Genet. 1988 Apr;4(4):106–111. doi: 10.1016/0168-9525(88)90098-4. [DOI] [PubMed] [Google Scholar]
- DeSalle R., Giddings L. V. Discordance of nuclear and mitochondrial DNA phylogenies in Hawaiian Drosophila. Proc Natl Acad Sci U S A. 1986 Sep;83(18):6902–6906. doi: 10.1073/pnas.83.18.6902. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Eanes W. F., Ajioka J. W., Hey J., Wesley C. Restriction-map variation associated with the G6PD polymorphism in natural populations of Drosophila melanogaster. Mol Biol Evol. 1989 Jul;6(4):384–397. doi: 10.1093/oxfordjournals.molbev.a040555. [DOI] [PubMed] [Google Scholar]
- Ferris S. D., Sage R. D., Prager E. M., Ritte U., Wilson A. C. Mitochondrial DNA evolution in mice. Genetics. 1983 Nov;105(3):681–721. doi: 10.1093/genetics/105.3.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
- George M., Jr, Ryder O. A. Mitochondrial DNA evolution in the genus Equus. Mol Biol Evol. 1986 Nov;3(6):535–546. doi: 10.1093/oxfordjournals.molbev.a040414. [DOI] [PubMed] [Google Scholar]
- Hale L. R., Singh R. S. Mitochondrial DNA variation and genetic structure in populations of Drosophila melanogaster. Mol Biol Evol. 1987 Nov;4(6):622–637. doi: 10.1093/oxfordjournals.molbev.a040466. [DOI] [PubMed] [Google Scholar]
- Johnson M. J., Wallace D. C., Ferris S. D., Rattazzi M. C., Cavalli-Sforza L. L. Radiation of human mitochondria DNA types analyzed by restriction endonuclease cleavage patterns. J Mol Evol. 1983;19(3-4):255–271. doi: 10.1007/BF02099973. [DOI] [PubMed] [Google Scholar]
- Klukas C. K., Dawid I. B. Characterization and mapping of mitochondrial ribosomal RNA and mitochondrial DNA in Drosophila melanogaster. Cell. 1976 Dec;9(4 Pt 1):615–625. doi: 10.1016/0092-8674(76)90044-1. [DOI] [PubMed] [Google Scholar]
- Lansman R. A., Shade R. O., Shapira J. F., Avise J. C. The use of restriction endonucleases to measure mitochondrial DNA sequence relatedness in natural populations. III. Techniques and potential applications. J Mol Evol. 1981;17(4):214–226. doi: 10.1007/BF01732759. [DOI] [PubMed] [Google Scholar]
- Latorre A., Barrio E., Moya A., Ayala F. J. Mitochondrial DNA evolution in the Drosophila obscura group. Mol Biol Evol. 1988 Nov;5(6):717–728. doi: 10.1093/oxfordjournals.molbev.a040526. [DOI] [PubMed] [Google Scholar]
- Oakeshott J. G., Chambers G. K., Gibson J. B., Willcocks D. A. Latitudinal relationships of esterase-6 and phosphoglucomutase gene frequencies in Drosophila melanogaster. Heredity (Edinb) 1981 Dec;47(Pt 3):385–396. doi: 10.1038/hdy.1981.99. [DOI] [PubMed] [Google Scholar]
- Ovenden J. R., White R. W. Mitochondrial and allozyme genetics of incipient speciation in a landlocked population of Galaxias truttaceus (Pisces: Galaxiidae). Genetics. 1990 Mar;124(3):701–716. doi: 10.1093/genetics/124.3.701. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Powers T. O., Platzer E. G., Hyman B. C. Large mitochondrial genome and mitochondrial DNA size polymorphism in the mosquito parasite, Romanomermis culicivorax. Curr Genet. 1986;11(1):71–77. doi: 10.1007/BF00389428. [DOI] [PubMed] [Google Scholar]
- Reeb C. A., Avise J. C. A genetic discontinuity in a continuously distributed species: mitochondrial DNA in the American oyster, Crassostrea virginica. Genetics. 1990 Feb;124(2):397–406. doi: 10.1093/genetics/124.2.397. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Singh G., Neckelmann N., Wallace D. C. Conformational mutations in human mitochondrial DNA. Nature. 1987 Sep 17;329(6136):270–272. doi: 10.1038/329270a0. [DOI] [PubMed] [Google Scholar]
- Singh R. S., Coulthart M. B. Genic variation in abundant soluble proteins of Drosophila melanogaster and Drosophila pseudoobscura. Genetics. 1982 Nov;102(3):437–453. doi: 10.1093/genetics/102.3.437. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Singh R. S., Hickey D. A., David J. Genetic Differentiation between Geographically Distant Populations of DROSOPHILA MELANOGASTER. Genetics. 1982 Jun;101(2):235–256. doi: 10.1093/genetics/101.2.235. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Singh R. S., Rhomberg L. R. A Comprehensive Study of Genic Variation in Natural Populations of Drosophila melanogaster. II. Estimates of Heterozygosity and Patterns of Geographic Differentiation. Genetics. 1987 Oct;117(2):255–271. doi: 10.1093/genetics/117.2.255. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wallis G. P. Mitochondrial DNA insertion polymorphism and germ line heteroplasmy in the Triturus cristatus complex. Heredity (Edinb) 1987 Apr;58(Pt 2):229–238. doi: 10.1038/hdy.1987.37. [DOI] [PubMed] [Google Scholar]
- Wolstenholme D. R., Dawid I. B. A size difference between mitochondrial DNA molecules of urodele and anuran amphibia. J Cell Biol. 1968 Oct;39(1):222–228. doi: 10.1083/jcb.39.1.222. [DOI] [PMC free article] [PubMed] [Google Scholar]
- de Bruijn M. H. Drosophila melanogaster mitochondrial DNA, a novel organization and genetic code. Nature. 1983 Jul 21;304(5923):234–241. doi: 10.1038/304234a0. [DOI] [PubMed] [Google Scholar]