Evolution of Hybrid Incompatibilities

 

It is widely believed that the normal course of evolution within isolated or semi-isolated populations gives rise to genetic incompatibilities that cause hybrid sterility or inviability resulting in new, reproductively isolated species. Because reproductive isolation typically involves multiple genetic incompatibilities, few experimental systems have been developed in which the genes underlying the incompatibilities can be isolated individually. One promising system makes use of introgression, in which various sized pieces of the genome of one species are introduced into the genome of another species. In our case the species are Drosophila mauritiana and D. simulans. The biological resource represented by these introgression lines provides the material to isolate and identify specific genes that are associated with hybrid male sterility in order to determine their origin (point mutation, gene fusion, transposition, duplication), their molecular evolution, and their misexpression in hybrids.

 

We used marked P-element insertions as dominant markers to efficiently identify a genetic region causing a severe reduction in fertility in hybrid males of D. simulans and D. mauritiana. The region contains two strong candidate genes: Taf1, a large gene whose product has sequence-specific DNA binding and transcription factor activity; and agt, a small, intronless gene, whose molecular function is annotated as methylated-DNA-protein-cysteine S-methyltransferase activity. The gene trees of both genes perfectly separate D. simulans and D. mauritiana into monophyletic groups, and we are currently creating transgenic lines and carrying other experiments to determine which of the genes is a hybrid male sterility factor.

 

The P-element introgressions also uncovered a cryptic system of sex-ratio distortion in D. simulans. In this case, a newly evolved X-linked gene we call Dox evolved the ability to distort the X chromosome in XY males, with the result that a Dox-bearing male produces about 80 percent female progeny. At the population level, this level of distortion imposes strong selection for suppressors. Consistent with this prediction, we have also discovered a newly evolved third-chromosomal gene we call Nmy that suppresses Dox. The Nmy suppressor appears to encode a microRNA. We are currently studying the mechanism and evolution of Dox and Nmy, and have evidence for a very recent strong selective sweep in the region of both genes.

 

  • Araripe, L. O., H. Montenegro, B. Lemos and D. L. Hartl, 2010 Fine-scale genetic mapping of a hybrid sterility factor between Drosophila simulans and D. mauritiana: The varied and elusive functions of "speciation genes." BMC Evol. Biol. 10: 385.
  • Kingan, S. B., D. Garrigan and D. L. Hartl, 2010 Recurrent selection on the Winters sex-ratio genes in Drosophila simulans. Genetics 184: 253–265.
  • Tao, Y., L. Araripe, S. B. Kingan, Y. Ke, H. Xiao, and D. L. Hartl. 2007. A sex-ratio meiotic drive system in Drosophila simulans. II: an X-linked distorter. PLoS Biol. 5:e293.
  • Tao, Y., J. P. Masly, L. Araripe, Y. Ke, and D. L. Hartl. 2007. A sex-ratio meiotic drive system in Drosophila simulans. I: an autosomal suppressor. PLoS Biol. 5:e292.
  • Landry, C. R., D. L. Hartl, and J. M. Ranz. 2007. Genome clashes in hybrids: insights from gene expression. Heredity. 99:483-493.