Haldane's Rule Is Linked to Extraordinary Sex Ratios and Sperm Length in Stalk-Eyed Flies
Gerald S. Wilkinson, Sarah J. Christianson, Cara L. Brand, George Ru, Wyatt Shell

Abstract

We use three allopatric populations of the stalk-eyed fly Teleopsis dalmanni from Southeast Asia to test two predictions made by the sex chromosome drive hypothesis for Haldane's rule. The first is that modifiers that suppress or enhance drive should evolve rapidly and independently in isolated populations. The second is that drive loci or modifiers should also cause sterility in hybrid males. We tested these predictions by assaying the fertility of 2,066 males derived from backcross experiments involving two pairs of populations and found that the proportion of mated males that fail to produce any offspring ranged from 38-60% among crosses with some males producing strongly female-biased or male-biased sex ratios. After genotyping each male at 25-28 genetic markers we found quantitative trait loci (QTL) that jointly influence male sterility, sperm length and biased progeny sex ratios in each pair of populations, but almost no shared QTL between population crosses. We also discovered that the extant XSR chromosome has no effect on sex ratio or sterility in these backcross males. Whether shared QTL are caused by linkage or pleiotropy requires additional study. Nevertheless, these results indicate the presence of a "cryptic" drive system that is currently masked by suppressing elements that are associated with sterility and sperm length within but not between populations and, therefore, must have evolved since the populations became isolated, i.e. in less than 100,000 years. We discuss how genes that influence sperm length may contribute to hybrid sterility.

  • Received June 19, 2014.
  • Accepted August 18, 2014.