Skip to main content
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2000 Aug 7;267(1452):1487–1495. doi: 10.1098/rspb.2000.1169

Evolutionary novelties in islands: Drosophila santomea, a new melanogaster sister species from São Tomé.

D Lachaise 1, M Harry 1, M Solignac 1, F Lemeunier 1, V Bénassi 1, M L Cariou 1
PMCID: PMC1690712  PMID: 11007323

Abstract

The finding of new melanogaster sister species may help us in understanding more about how the emergence of genetic novelties, particularly in insular habitats, can result in speciation. Here we report on the discovery of Drosophila santomea, which is the first melanogaster sibling found off West-equatorial Africa, on São Tomé, one of the Gulf of Guinea islands. Although the eight other melanogaster sister species are remarkably conservative in their morphology except for their terminalia, the new find has a morphological trait distinguishing it from all of these: a pure yellow body coloration of both sexes without the normal black abdominal banding. Evidence from the terminalia, polytene and mitotic chromosomes, period gene and allozymes are provided indicating that it is nonetheless the nearest relative of Drosophila yakuba with which it coexists on the island. The new find is a clear-cut taxon as shown by the production of sterile male hybrids, eventually with developmental defects, in both directions of cross with yakuba and by the existence of an altitudinal divide accompanied by a hybrid zone at mid-elevation on the island. Molecular and karyotypic data further support this conclusion. In contrast to the significant divergence of their nuclear DNAs, an intriguing similarity in their cytochrome b sequences was observed indicating a recent coalescence common to santomea, yakuba and also teissieri cytoplasms. These were shown to harbour the same Wolbachia endosymbiotic bacteria which could possibly be responsible for mitochondrial DNA hitchhiking across the species barrier.

Full Text

The Full Text of this article is available as a PDF (718.4 KB).

Selected References

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

  1. Adams M. D., Celniker S. E., Holt R. A., Evans C. A., Gocayne J. D., Amanatides P. G., Scherer S. E., Li P. W., Hoskins R. A., Galle R. F. The genome sequence of Drosophila melanogaster. Science. 2000 Mar 24;287(5461):2185–2195. doi: 10.1126/science.287.5461.2185. [DOI] [PubMed] [Google Scholar]
  2. Ashburner M., Misra S., Roote J., Lewis S. E., Blazej R., Davis T., Doyle C., Galle R., George R., Harris N. An exploration of the sequence of a 2.9-Mb region of the genome of Drosophila melanogaster: the Adh region. Genetics. 1999 Sep;153(1):179–219. doi: 10.1093/genetics/153.1.179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Avise J. C., Walker D., Johns G. C. Speciation durations and Pleistocene effects on vertebrate phylogeography. Proc Biol Sci. 1998 Sep 22;265(1407):1707–1712. doi: 10.1098/rspb.1998.0492. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Avise J. C., Walker D. Pleistocene phylogeographic effects on avian populations and the speciation process. Proc Biol Sci. 1998 Mar 22;265(1395):457–463. doi: 10.1098/rspb.1998.0317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Barton N. H., Hewitt G. M. Adaptation, speciation and hybrid zones. Nature. 1989 Oct 12;341(6242):497–503. doi: 10.1038/341497a0. [DOI] [PubMed] [Google Scholar]
  6. Barton N. H. Natural selection and random genetic drift as causes of evolution on islands. Philos Trans R Soc Lond B Biol Sci. 1996 Jun 29;351(1341):785–795. doi: 10.1098/rstb.1996.0073. [DOI] [PubMed] [Google Scholar]
  7. Bourtzis K., Dobson S. L., Braig H. R., O'Neill S. L. Rescuing Wolbachia have been overlooked. Nature. 1998 Feb 26;391(6670):852–853. doi: 10.1038/36017. [DOI] [PubMed] [Google Scholar]
  8. Braig H. R., Zhou W., Dobson S. L., O'Neill S. L. Cloning and characterization of a gene encoding the major surface protein of the bacterial endosymbiont Wolbachia pipientis. J Bacteriol. 1998 May;180(9):2373–2378. doi: 10.1128/jb.180.9.2373-2378.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cariou M. L. Biochemical phylogeny of the eight species in the Drosophila melanogaster subgroup, including D. sechellia and D. orena. Genet Res. 1987 Dec;50(3):181–185. doi: 10.1017/s0016672300023673. [DOI] [PubMed] [Google Scholar]
  10. Carson H. L. The Wilhelmine E. Key 1996 Invitational Lecture. Sexual selection: a driver of genetic change in Hawaiian Drosophila. J Hered. 1997 Sep-Oct;88(5):343–352. doi: 10.1093/oxfordjournals.jhered.a023115. [DOI] [PubMed] [Google Scholar]
  11. Citri Y., Colot H. V., Jacquier A. C., Yu Q., Hall J. C., Baltimore D., Rosbash M. A family of unusually spliced biologically active transcripts encoded by a Drosophila clock gene. Nature. 1987 Mar 5;326(6108):42–47. doi: 10.1038/326042a0. [DOI] [PubMed] [Google Scholar]
  12. Clary D. O., Wolstenholme D. R. The mitochondrial DNA molecular of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. J Mol Evol. 1985;22(3):252–271. doi: 10.1007/BF02099755. [DOI] [PubMed] [Google Scholar]
  13. Coyne J. A., Charlesworth B. Genetics of a pheromonal difference affecting sexual isolation between Drosophila mauritiana and D. sechellia. Genetics. 1997 Apr;145(4):1015–1030. doi: 10.1093/genetics/145.4.1015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Coyne J. A. Genetics and speciation. Nature. 1992 Feb 6;355(6360):511–515. doi: 10.1038/355511a0. [DOI] [PubMed] [Google Scholar]
  15. Coyne J. A. Genetics of sexual isolation between two sibling species, Drosophila simulans and Drosophila mauritiana. Proc Natl Acad Sci U S A. 1989 Jul;86(14):5464–5468. doi: 10.1073/pnas.86.14.5464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Coyne J. A. The genetic basis of Haldane's rule. 1985 Apr 25-May 1Nature. 314(6013):736–738. doi: 10.1038/314736a0. [DOI] [PubMed] [Google Scholar]
  17. Davis A. W., Roote J., Morley T., Sawamura K., Herrmann S., Ashburner M. Rescue of hybrid sterility in crosses between D. melanogaster and D. simulans. Nature. 1996 Mar 14;380(6570):157–159. doi: 10.1038/380157a0. [DOI] [PubMed] [Google Scholar]
  18. Fleischer R. C., McIntosh C. E., Tarr C. L. Evolution on a volcanic conveyor belt: using phylogeographic reconstructions and K-Ar-based ages of the Hawaiian Islands to estimate molecular evolutionary rates. Mol Ecol. 1998 Apr;7(4):533–545. doi: 10.1046/j.1365-294x.1998.00364.x. [DOI] [PubMed] [Google Scholar]
  19. Galtier N., Gouy M., Gautier C. SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci. 1996 Dec;12(6):543–548. doi: 10.1093/bioinformatics/12.6.543. [DOI] [PubMed] [Google Scholar]
  20. Gleason J. M., Powell J. R. Interspecific and intraspecific comparisons of the period locus in the Drosophila willistoni sibling species. Mol Biol Evol. 1997 Jul;14(7):741–753. doi: 10.1093/oxfordjournals.molbev.a025814. [DOI] [PubMed] [Google Scholar]
  21. Halder G., Callaerts P., Gehring W. J. Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science. 1995 Mar 24;267(5205):1788–1792. doi: 10.1126/science.7892602. [DOI] [PubMed] [Google Scholar]
  22. Harry M., Solignac M., Lachaise D. Molecular evidence for parallel evolution of adaptive syndromes in fig-breeding Lissocephala (Drosophilidae). Mol Phylogenet Evol. 1998 Jun;9(3):542–551. doi: 10.1006/mpev.1998.0508. [DOI] [PubMed] [Google Scholar]
  23. Khadem M., Krimbas C. B. Studies of the species barrier between Drosophila madeirensis and Drosophila subobscura. II. Genetic analysis of developmental incompatibilities in hybrids. Hereditas. 1991;114(2):189–195. doi: 10.1111/j.1601-5223.1991.tb00323.x. [DOI] [PubMed] [Google Scholar]
  24. Long M., Langley C. H. Natural selection and the origin of jingwei, a chimeric processed functional gene in Drosophila. Science. 1993 Apr 2;260(5104):91–95. doi: 10.1126/science.7682012. [DOI] [PubMed] [Google Scholar]
  25. Markow T. A., Ricker J. P. Developmental stability in hybrids between the sibling species pair, Drosophila melanogaster and Drosophila simulans. Genetica. 1991;84(2):115–121. doi: 10.1007/BF00116551. [DOI] [PubMed] [Google Scholar]
  26. Merçot H., Poinsot D. . . . and discovered on Mount Kilimanjaro. Nature. 1998 Feb 26;391(6670):853–853. doi: 10.1038/36021. [DOI] [PubMed] [Google Scholar]
  27. Monnerot M., Solignac M., Wolstenholme D. R. Discrepancy in divergence of the mitochondrial and nuclear genomes of Drosophila teissieri and Drosophila yakuba. J Mol Evol. 1990 Jun;30(6):500–508. doi: 10.1007/BF02101105. [DOI] [PubMed] [Google Scholar]
  28. Orr H. A. Developmental anomalies in Drosophila hybrids are apparently caused by loss of microchromosome. Heredity (Edinb) 1990 Apr;64(Pt 2):255–262. doi: 10.1038/hdy.1990.31. [DOI] [PubMed] [Google Scholar]
  29. doi: 10.1098/rstb.1998.0206. [DOI] [PMC free article] [Google Scholar]
  30. Peixoto A. A., Costa R., Wheeler D. A., Hall J. C., Kyriacou C. P. Evolution of the threonine-glycine repeat region of the period gene in the melanogaster species subgroup of Drosophila. J Mol Evol. 1992 Nov;35(5):411–419. doi: 10.1007/BF00171819. [DOI] [PubMed] [Google Scholar]
  31. Rousset F., Solignac M. Evolution of single and double Wolbachia symbioses during speciation in the Drosophila simulans complex. Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6389–6393. doi: 10.1073/pnas.92.14.6389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Rousset F., Vautrin D., Solignac M. Molecular identification of Wolbachia, the agent of cytoplasmic incompatibility in Drosophila simulans, and variability in relation with host mitochondrial types. Proc Biol Sci. 1992 Mar 23;247(1320):163–168. doi: 10.1098/rspb.1992.0023. [DOI] [PubMed] [Google Scholar]
  33. Rutherford S. L., Lindquist S. Hsp90 as a capacitor for morphological evolution. Nature. 1998 Nov 26;396(6709):336–342. doi: 10.1038/24550. [DOI] [PubMed] [Google Scholar]
  34. Sawamura K., Davis A. W., Wu C. I. Genetic analysis of speciation by means of introgression into Drosophila melanogaster. Proc Natl Acad Sci U S A. 2000 Mar 14;97(6):2652–2655. doi: 10.1073/pnas.050558597. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Spradling A. C., Stern D., Beaton A., Rhem E. J., Laverty T., Mozden N., Misra S., Rubin G. M. The Berkeley Drosophila Genome Project gene disruption project: Single P-element insertions mutating 25% of vital Drosophila genes. Genetics. 1999 Sep;153(1):135–177. doi: 10.1093/genetics/153.1.135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sánchez L., Santamaria P. Reproductive isolation and morphogenetic evolution in Drosophila analyzed by breakage of ethological barriers. Genetics. 1997 Sep;147(1):231–242. doi: 10.1093/genetics/147.1.231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Thackeray J. R., Kyriacou C. P. Molecular evolution in the Drosophila yakuba period locus. J Mol Evol. 1990 Nov;31(5):389–401. doi: 10.1007/BF02106054. [DOI] [PubMed] [Google Scholar]
  38. Ting C. T., Tsaur S. C., Wu M. L., Wu C. I. A rapidly evolving homeobox at the site of a hybrid sterility gene. Science. 1998 Nov 20;282(5393):1501–1504. doi: 10.1126/science.282.5393.1501. [DOI] [PubMed] [Google Scholar]
  39. Wang D., Marsh J. L., Ayala F. J. Evolutionary changes in the expression pattern of a developmentally essential gene in three Drosophila species. Proc Natl Acad Sci U S A. 1996 Jul 9;93(14):7103–7107. doi: 10.1073/pnas.93.14.7103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Wu C. I., Hollocher H., Begun D. J., Aquadro C. F., Xu Y., Wu M. L. Sexual isolation in Drosophila melanogaster: a possible case of incipient speciation. Proc Natl Acad Sci U S A. 1995 Mar 28;92(7):2519–2523. doi: 10.1073/pnas.92.7.2519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Zhou W., Rousset F., O'Neil S. Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proc Biol Sci. 1998 Mar 22;265(1395):509–515. doi: 10.1098/rspb.1998.0324. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES