PgmNr P356: ­­­Evidence for the interspecies transfer of a driving X chromosome.

Authors:
C. Leonard 1 ; Z. Fuller 2 ; R. Young 1 ; S. Schaeffer 2 ; N. Phadnis 1


Institutes
1) University of Utah, Salt Lake City, UT; 2) Pennsylvania State University, State College, PA.


Abstract:

Segregation distorters are selfish genetic elements that gain an evolutionary advantage by fundamentally violating Mendel’s Laws of inheritance. Such distorting systems are found in a wide swath of eukaryotes and powerfully bias segregation ratios in their own favor. When sex chromosomes gain distorting elements, massive shifts to the population sex ratio may even drive populations or species to extinction. While the selective advantage for selfish segregation is obvious, the origins of these distorting chromosomes have proven much more enigmatic.

The Sex-Ratio (SR) chromosomes in Drosophila pseudoobscura and its sister species Drosophila persimilis are classic cases of distorting X chromosomes. Males that carry these distorting X chromosomes produce almost exclusively X-bearing sperm, disrupting the sex ratio of their progeny. These SR chromosomes exist as stable polymorphisms in wild populations; neither species has acquired suppressors to counter distortion in males. Perhaps most fascinating is the observation that the D. persimilis SR (DperSR) chromosome lacks a large inversion acquired on the standard D. persimilis X (DperST) chromosome, causing it to be collinear with the standard chromosome of D. pseudoobscura (DpseST). This collinearity is nearly or entirely complete, and it has been mapped down to a short array of repeats at either breakpoint. The simplest explanation for this strange collinearity between DperSR and DpseST is that the DperSR chromosome may have been derived through re-inversion at the same breakpoints to restore collinearity with DpseST.

Surprisingly, our results show that this is not the case. A sliding window phylogeny test across the X chromosome shows that DperSR clearly clusters with DpseST, forming a monophyletic group across species. This clustering is specifically found at the chromosomal inversion breakpoints, where recombination between DperSR and DperST is heavily limited. Through further statistical methods designed to detect gene flow between populations, we detect robust signatures of introgression between DpseST and DperSR. Together, our data suggest a recent origin for D. persimilis SR chromosome through transfer from D. pseudoobscura. While gene flow across species is halted by hybrid incompatibilities, this chromosome may have persisted in its sister species through its ability to distort. Thus, while distorting elements have been implicated in generating hybrid incompatibility, our work indicates that segregation distorters may also promote gene flow across species by conferring a strong selective advantage to an otherwise deleterious genotype.