Genetic architecture of a morphological shape difference between two Drosophila species (original) (raw)

Abstract

The size and shape of the posterior lobe of the male genital arch differs dramatically between Drosophila simulans and D. mauritiana. This difference can be quantified with a morphometric descriptor (PC1) based on elliptical Fourier and principal components analyses. The genetic basis of the interspecific difference in PC1 was investigated by the application of quantitative trait locus (QTL) mapping procedures to segregating backcross populations. The parental difference (35 environmental standard deviations) and the heritability of PC1 in backcross populations (>90%) are both very large. The use of multiple interval mapping gives evidence for 19 different QTL. The greatest additive effect estimate accounts for 11. 4% of the parental difference but could represent multiple closely linked QTL. Dominance parameter estimates vary among loci from essentially no dominance to complete dominance, and mauritiana alleles tend to be dominant over simulans alleles. Epistasis appears to be relatively unimportant as a source of variation. All but one of the additive effect estimates have the same sign, which means that one species has nearly all plus alleles and the other nearly all minus alleles. This result is unexpected under many evolutionary scenarios and suggests a history of strong directional selection acting on the posterior lobe.

Full Text

The Full Text of this article is available as a PDF (178.9 KB).

Selected References

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

  1. Alpert K. B., Tanksley S. D. High-resolution mapping and isolation of a yeast artificial chromosome contig containing fw2.2: a major fruit weight quantitative trait locus in tomato. Proc Natl Acad Sci U S A. 1996 Dec 24;93(26):15503–15507. doi: 10.1073/pnas.93.26.15503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Carroll S. B., Weatherbee S. D., Langeland J. A. Homeotic genes and the regulation and evolution of insect wing number. Nature. 1995 May 4;375(6526):58–61. doi: 10.1038/375058a0. [DOI] [PubMed] [Google Scholar]
  3. Cormier R. T., Hong K. H., Halberg R. B., Hawkins T. L., Richardson P., Mulherkar R., Dove W. F., Lander E. S. Secretory phospholipase Pla2g2a confers resistance to intestinal tumorigenesis. Nat Genet. 1997 Sep;17(1):88–91. doi: 10.1038/ng0997-88. [DOI] [PubMed] [Google Scholar]
  4. Hey J., Kliman R. M. Population genetics and phylogenetics of DNA sequence variation at multiple loci within the Drosophila melanogaster species complex. Mol Biol Evol. 1993 Jul;10(4):804–822. doi: 10.1093/oxfordjournals.molbev.a040044. [DOI] [PubMed] [Google Scholar]
  5. Iwasa Y., Pomiankowski A. Continual change in mate preferences. Nature. 1995 Oct 5;377(6548):420–422. doi: 10.1038/377420a0. [DOI] [PubMed] [Google Scholar]
  6. Jiang C., Zeng Z. B. Multiple trait analysis of genetic mapping for quantitative trait loci. Genetics. 1995 Jul;140(3):1111–1127. doi: 10.1093/genetics/140.3.1111. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Kao C. H., Zeng Z. B. General formulas for obtaining the MLEs and the asymptotic variance-covariance matrix in mapping quantitative trait loci when using the EM algorithm. Biometrics. 1997 Jun;53(2):653–665. [PubMed] [Google Scholar]
  8. Kao C. H., Zeng Z. B., Teasdale R. D. Multiple interval mapping for quantitative trait loci. Genetics. 1999 Jul;152(3):1203–1216. doi: 10.1093/genetics/152.3.1203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Lande R. Models of speciation by sexual selection on polygenic traits. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3721–3725. doi: 10.1073/pnas.78.6.3721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Liu J., Mercer J. M., Stam L. F., Gibson G. C., Zeng Z. B., Laurie C. C. Genetic analysis of a morphological shape difference in the male genitalia of Drosophila simulans and D. mauritiana. Genetics. 1996 Apr;142(4):1129–1145. doi: 10.1093/genetics/142.4.1129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Long A. D., Mullaney S. L., Reid L. A., Fry J. D., Langley C. H., Mackay T. F. High resolution mapping of genetic factors affecting abdominal bristle number in Drosophila melanogaster. Genetics. 1995 Mar;139(3):1273–1291. doi: 10.1093/genetics/139.3.1273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Maekawa B., Cole T. G., Seip R. L., Bylund D. Apolipoprotein E genotyping methods for the clinical laboratory. J Clin Lab Anal. 1995;9(1):63–69. doi: 10.1002/jcla.1860090112. [DOI] [PubMed] [Google Scholar]
  13. Orr H. A. Testing natural selection vs. genetic drift in phenotypic evolution using quantitative trait locus data. Genetics. 1998 Aug;149(4):2099–2104. doi: 10.1093/genetics/149.4.2099. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Saiki R. K., Bugawan T. L., Horn G. T., Mullis K. B., Erlich H. A. Analysis of enzymatically amplified beta-globin and HLA-DQ alpha DNA with allele-specific oligonucleotide probes. Nature. 1986 Nov 13;324(6093):163–166. doi: 10.1038/324163a0. [DOI] [PubMed] [Google Scholar]
  15. Shubin N., Tabin C., Carroll S. Fossils, genes and the evolution of animal limbs. Nature. 1997 Aug 14;388(6643):639–648. doi: 10.1038/41710. [DOI] [PubMed] [Google Scholar]
  16. Tanksley S. D. Mapping polygenes. Annu Rev Genet. 1993;27:205–233. doi: 10.1146/annurev.ge.27.120193.001225. [DOI] [PubMed] [Google Scholar]
  17. deVicente M. C., Tanksley S. D. QTL analysis of transgressive segregation in an interspecific tomato cross. Genetics. 1993 Jun;134(2):585–596. doi: 10.1093/genetics/134.2.585. [DOI] [PMC free article] [PubMed] [Google Scholar]