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Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2003 Jun 7;270(1520):1193–1202. doi: 10.1098/rspb.2003.2333

The causes of phylogenetic conflict in a classic Drosophila species group.

Carlos A Machado 1, Jody Hey 1
PMCID: PMC1691361  PMID: 12816659

Abstract

Bifurcating phylogenies are frequently used to describe the evolutionary history of groups of related species. However, simple bifurcating models may poorly represent the evolutionary history of species that have been exchanging genes. Here, we show that the history of three well-known closely related species, Drosophila pseudoobscura, D. persimilis and D. p. bogotana, is not well represented by a bifurcating phylogenetic tree. The phylogenetic relationships among these species vary widely between different genomic regions. Much of this phylogenetic variation can be explained by the potential of different genomic regions to introgress between species, as measured in laboratory studies. We argue that the utility of multiple markers in species-level phylogenetic studies can be greatly enhanced by knowledge of genomic location and, in the case of hybridizing species, by knowledge of the functional or linkage relationships among the markers and regions of the genome that reduce hybrid fitness.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ayala F. J., Powell J. R. Allozymes as diagnostic characters of sibling species of Drosophila. Proc Natl Acad Sci U S A. 1972 May;69(5):1094–1096. doi: 10.1073/pnas.69.5.1094. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brower A. V. Rapid morphological radiation and convergence among races of the butterfly Heliconius erato inferred from patterns of mitochondrial DNA evolution. Proc Natl Acad Sci U S A. 1994 Jul 5;91(14):6491–6495. doi: 10.1073/pnas.91.14.6491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Charlesworth B., Morgan M. T., Charlesworth D. The effect of deleterious mutations on neutral molecular variation. Genetics. 1993 Aug;134(4):1289–1303. doi: 10.1093/genetics/134.4.1289. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. DOBZHANSKY T., HUNTER A. S., PAVLOVSKY O., SPASSKY B., WALLACE B. Genetics of natural populations. XXXI. Genetics of an isolated marginal population of Drosophila pseudoobscura. Genetics. 1963 Jan;48:91–103. doi: 10.1093/genetics/48.1.91. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dobzhansky T. Studies on Hybrid Sterility. II. Localization of Sterility Factors in Drosophila Pseudoobscura Hybrids. Genetics. 1936 Mar;21(2):113–135. doi: 10.1093/genetics/21.2.113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Fu Y. X., Li W. H. Statistical tests of neutrality of mutations. Genetics. 1993 Mar;133(3):693–709. doi: 10.1093/genetics/133.3.693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hudson R. R. Gene trees, species trees and the segregation of ancestral alleles. Genetics. 1992 Jun;131(2):509–513. doi: 10.1093/genetics/131.2.509. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hudson R. R., Kreitman M., Aguadé M. A test of neutral molecular evolution based on nucleotide data. Genetics. 1987 May;116(1):153–159. doi: 10.1093/genetics/116.1.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hudson R. R., Slatkin M., Maddison W. P. Estimation of levels of gene flow from DNA sequence data. Genetics. 1992 Oct;132(2):583–589. doi: 10.1093/genetics/132.2.583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hudson Richard R., Coyne Jerry A. Mathematical consequences of the genealogical species concept. Evolution. 2002 Aug;56(8):1557–1565. doi: 10.1111/j.0014-3820.2002.tb01467.x. [DOI] [PubMed] [Google Scholar]
  11. Hutter C. M., Rand D. M. Competition between mitochondrial haplotypes in distinct nuclear genetic environments: Drosophila pseudoobscura vs. D. persimilis. Genetics. 1995 Jun;140(2):537–548. doi: 10.1093/genetics/140.2.537. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kumar S., Tamura K., Jakobsen I. B., Nei M. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics. 2001 Dec;17(12):1244–1245. doi: 10.1093/bioinformatics/17.12.1244. [DOI] [PubMed] [Google Scholar]
  13. Machado Carlos A., Kliman Richard M., Markert Jeffrey A., Hey Jody. 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):472–488. doi: 10.1093/oxfordjournals.molbev.a004103. [DOI] [PubMed] [Google Scholar]
  14. Noor M. A., Grams K. L., Bertucci L. A., Almendarez Y., Reiland J., Smith K. R. The genetics of reproductive isolation and the potential for gene exchange between Drosophila pseudoobscura and D. persimilis via backcross hybrid males. Evolution. 2001 Mar;55(3):512–521. doi: 10.1554/0014-3820(2001)055[0512:tgoria]2.0.co;2. [DOI] [PubMed] [Google Scholar]
  15. Orr H. A. Genetics of male and female sterility in hybrids of Drosophila pseudoobscura and D. persimilis. Genetics. 1987 Aug;116(4):555–563. doi: 10.1093/genetics/116.4.555. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Pamilo P., Nei M. Relationships between gene trees and species trees. Mol Biol Evol. 1988 Sep;5(5):568–583. doi: 10.1093/oxfordjournals.molbev.a040517. [DOI] [PubMed] [Google Scholar]
  17. Powell J. R. Interspecific cytoplasmic gene flow in the absence of nuclear gene flow: evidence from Drosophila. Proc Natl Acad Sci U S A. 1983 Jan;80(2):492–495. doi: 10.1073/pnas.80.2.492. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Powell J. R. Monophyly/paraphyly/polyphyly and gene/species trees: an example from Drosophila. Mol Biol Evol. 1991 Nov;8(6):892–896. doi: 10.1093/oxfordjournals.molbev.a040695. [DOI] [PubMed] [Google Scholar]
  19. Prakash S. Origin of reproductive isolation in the absence of apparent genic differentiation in a geographic isolate of Drosophila pseudoobscura. Genetics. 1972 Sep;72(1):143–155. doi: 10.1093/genetics/72.1.143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Schaeffer S. W., Miller E. L. Nucleotide sequence analysis of Adh genes estimates the time of geographic isolation of the Bogota population of Drosophila pseudoobscura. Proc Natl Acad Sci U S A. 1991 Jul 15;88(14):6097–6101. doi: 10.1073/pnas.88.14.6097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Slatkin M., Maddison W. P. A cladistic measure of gene flow inferred from the phylogenies of alleles. Genetics. 1989 Nov;123(3):603–613. doi: 10.1093/genetics/123.3.603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Smith J. M., Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed] [Google Scholar]
  24. Sota T., Vogler A. P. Incongruence of mitochondrial and nuclear gene trees in the Carabid beetles Ohomopterus. Syst Biol. 2001 Feb;50(1):39–59. [PubMed] [Google Scholar]
  25. Stephan W., Xing L., Kirby D. A., Braverman J. M. A test of the background selection hypothesis based on nucleotide data from Drosophila ananassae. Proc Natl Acad Sci U S A. 1998 May 12;95(10):5649–5654. doi: 10.1073/pnas.95.10.5649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Tajima F. Evolutionary relationship of DNA sequences in finite populations. Genetics. 1983 Oct;105(2):437–460. doi: 10.1093/genetics/105.2.437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989 Nov;123(3):585–595. doi: 10.1093/genetics/123.3.585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Takahata N. Gene genealogy in three related populations: consistency probability between gene and population trees. Genetics. 1989 Aug;122(4):957–966. doi: 10.1093/genetics/122.4.957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Wang R. L., Hey J. The speciation history of Drosophila pseudoobscura and close relatives: inferences from DNA sequence variation at the period locus. Genetics. 1996 Nov;144(3):1113–1126. doi: 10.1093/genetics/144.3.1113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wang R. L., Wakeley J., Hey J. Gene flow and natural selection in the origin of Drosophila pseudoobscura and close relatives. Genetics. 1997 Nov;147(3):1091–1106. doi: 10.1093/genetics/147.3.1091. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Watterson G. A. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 1975 Apr;7(2):256–276. doi: 10.1016/0040-5809(75)90020-9. [DOI] [PubMed] [Google Scholar]
  33. Wu C. I. Inferences of species phylogeny in relation to segregation of ancient polymorphisms. Genetics. 1991 Feb;127(2):429–435. doi: 10.1093/genetics/127.2.429. [DOI] [PMC free article] [PubMed] [Google Scholar]

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