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. 1996 Sep;144(1):427–437. doi: 10.1093/genetics/144.1.427

Heterozygosity, Heteromorphy, and Phylogenetic Trees in Asexual Eukaryotes

C W Birky-Jr 1
PMCID: PMC1207515  PMID: 8878706

Abstract

Little attention has been paid to the consequences of long-term asexual reproduction for sequence evolution in diploid or polyploid eukaryotic organisms. Some elementary theory shows that the amount of neutral sequence divergence between two alleles of a protein-coding gene in an asexual individual will be greater than that in a sexual species by a factor of 2tu, where t is the number of generations since sexual reproduction was lost and u is the mutation rate per generation in the asexual lineage. Phylogenetic trees based on only one allele from each of two or more species will show incorrect divergence times and, more often than not, incorrect topologies. This allele sequence divergence can be stopped temporarily by mitotic gene conversion, mitotic crossing-over, or ploidy reduction. If these convergence events are rare, ancient asexual lineages can be recognized by their high allele sequence divergence. At intermediate frequencies of convergence events, it will be impossible to reconstruct the correct phylogeny of an asexual clade from the sequences of protein coding genes. Convergence may be limited by allele sequence divergence and heterozygous chromosomal rearrangements which reduce the homology needed for recombination and result in aneuploidy after crossing-over or ploidy cycles.

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Selected References

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  1. Adam R. D. Chromosome-size variation in Giardia lamblia: the role of rDNA repeats. Nucleic Acids Res. 1992 Jun 25;20(12):3057–3061. doi: 10.1093/nar/20.12.3057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barns S. M., Lane D. J., Sogin M. L., Bibeau C., Weisburg W. G. Evolutionary relationships among pathogenic Candida species and relatives. J Bacteriol. 1991 Apr;173(7):2250–2255. doi: 10.1128/jb.173.7.2250-2255.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Byers T. J., Hugo E. R., Stewart V. J. Genes of Acanthamoeba: DNA, RNA and protein sequences (a review). J Protozool. 1990 Jul-Aug;37(4):17S–25S. doi: 10.1111/j.1550-7408.1990.tb01141.x. [DOI] [PubMed] [Google Scholar]
  4. Caugant D. A., Sandven P. Epidemiological analysis of Candida albicans strains by multilocus enzyme electrophoresis. J Clin Microbiol. 1993 Feb;31(2):215–220. doi: 10.1128/jcm.31.2.215-220.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chu W. S., Magee B. B., Magee P. T. Construction of an SfiI macrorestriction map of the Candida albicans genome. J Bacteriol. 1993 Oct;175(20):6637–6651. doi: 10.1128/jb.175.20.6637-6651.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. García-Bellido A., Wandosell F. The effect of inversions on mitotic recombination in Drosophila melanogaster. Mol Gen Genet. 1978 May 31;161(3):317–321. doi: 10.1007/BF00331007. [DOI] [PubMed] [Google Scholar]
  7. Glassberg J., Miyazaki L., Rifkin M. R. Isolation and partial characterization of mutants of the trypanosomatid Crithidia fasciculata and their use in detecting genetic recombination. J Protozool. 1985 Feb;32(1):118–125. doi: 10.1111/j.1550-7408.1985.tb03025.x. [DOI] [PubMed] [Google Scholar]
  8. Golic M. M., Golic K. G. A quantitative measure of the mitotic pairing of alleles in Drosophila melanogaster and the influence of structural heterozygosity. Genetics. 1996 May;143(1):385–400. doi: 10.1093/genetics/143.1.385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Harris H. Enzyme polymorphisms in man. Proc R Soc Lond B Biol Sci. 1966 Mar 22;164(995):298–310. doi: 10.1098/rspb.1966.0032. [DOI] [PubMed] [Google Scholar]
  10. Hickey D. A. Selfish DNA: a sexually-transmitted nuclear parasite. Genetics. 1982 Jul-Aug;101(3-4):519–531. doi: 10.1093/genetics/101.3-4.519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hilliker A. J., Harauz G., Reaume A. G., Gray M., Clark S. H., Chovnick A. Meiotic gene conversion tract length distribution within the rosy locus of Drosophila melanogaster. Genetics. 1994 Aug;137(4):1019–1026. doi: 10.1093/genetics/137.4.1019. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hubby J. L., Lewontin R. C. A molecular approach to the study of genic heterozygosity in natural populations. I. The number of alleles at different loci in Drosophila pseudoobscura. Genetics. 1966 Aug;54(2):577–594. doi: 10.1093/genetics/54.2.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Jenni L., Marti S., Schweizer J., Betschart B., Le Page R. W., Wells J. M., Tait A., Paindavoine P., Pays E., Steinert M. Hybrid formation between African trypanosomes during cyclical transmission. Nature. 1986 Jul 10;322(6075):173–175. doi: 10.1038/322173a0. [DOI] [PubMed] [Google Scholar]
  14. Kondrashov A. S. Mutation load under vegetative reproduction and cytoplasmic inheritance. Genetics. 1994 May;137(1):311–318. doi: 10.1093/genetics/137.1.311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kreitman M. Nucleotide polymorphism at the alcohol dehydrogenase locus of Drosophila melanogaster. Nature. 1983 Aug 4;304(5925):412–417. doi: 10.1038/304412a0. [DOI] [PubMed] [Google Scholar]
  16. Lynch M., Bürger R., Butcher D., Gabriel W. The mutational meltdown in asexual populations. J Hered. 1993 Sep-Oct;84(5):339–344. doi: 10.1093/oxfordjournals.jhered.a111354. [DOI] [PubMed] [Google Scholar]
  17. Moriyama E. N., Powell J. R. Intraspecific nuclear DNA variation in Drosophila. Mol Biol Evol. 1996 Jan;13(1):261–277. doi: 10.1093/oxfordjournals.molbev.a025563. [DOI] [PubMed] [Google Scholar]
  18. Ohkuma M., Hwang C. W., Masuda Y., Nishida H., Sugiyama J., Ohta A., Takagi M. Evolutionary position of n-alkane-assimilating yeast Candida maltosa shown by nucleotide sequence of small-subunit ribosomal RNA gene. Biosci Biotechnol Biochem. 1993 Oct;57(10):1793–1794. doi: 10.1271/bbb.57.1793. [DOI] [PubMed] [Google Scholar]
  19. Ohkuma M., Muraoka S., Hwang C. W., Ohta A., Takagi M. Cloning of the C-URA3 gene and construction of a triple auxotroph (his5, ade1, ura3) as a useful host for the genetic engineering of Candida maltosa. Curr Genet. 1993 Mar;23(3):205–210. doi: 10.1007/BF00351497. [DOI] [PubMed] [Google Scholar]
  20. Ohkuma M., Muraoka S., Tanimoto T., Fujii M., Ohta A., Takagi M. CYP52 (cytochrome P450alk) multigene family in Candida maltosa: identification and characterization of eight members. DNA Cell Biol. 1995 Feb;14(2):163–173. doi: 10.1089/dna.1995.14.163. [DOI] [PubMed] [Google Scholar]
  21. Pujol C., Reynes J., Renaud F., Raymond M., Tibayrenc M., Ayala F. J., Janbon F., Mallié M., Bastide J. M. The yeast Candida albicans has a clonal mode of reproduction in a population of infected human immunodeficiency virus-positive patients. Proc Natl Acad Sci U S A. 1993 Oct 15;90(20):9456–9459. doi: 10.1073/pnas.90.20.9456. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Thomas B. J., Rothstein R. Sex, maps, and imprinting. Cell. 1991 Jan 11;64(1):1–3. doi: 10.1016/0092-8674(91)90199-9. [DOI] [PubMed] [Google Scholar]
  23. Thrash-Bingham C., Gorman J. A. DNA translocations contribute to chromosome length polymorphisms in Candida albicans. Curr Genet. 1992 Aug;22(2):93–100. doi: 10.1007/BF00351467. [DOI] [PubMed] [Google Scholar]
  24. Tibayrenc M., Kjellberg F., Arnaud J., Oury B., Brenière S. F., Dardé M. L., Ayala F. J. Are eukaryotic microorganisms clonal or sexual? A population genetics vantage. Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5129–5133. doi: 10.1073/pnas.88.12.5129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. van Keulen H., Gutell R. R., Gates M. A., Campbell S. R., Erlandsen S. L., Jarroll E. L., Kulda J., Meyer E. A. Unique phylogenetic position of Diplomonadida based on the complete small subunit ribosomal RNA sequence of Giardia ardeae, G. muris, G. duodenalis and Hexamita sp. FASEB J. 1993 Jan;7(1):223–231. doi: 10.1096/fasebj.7.1.8422968. [DOI] [PubMed] [Google Scholar]

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