Reproductive isolation and X chromosome meiotic drive in Cyrtodiopsis stalk-eyed flies

Abstract

Haldane's rule states that when one sex of hybrids shows sterility or inviability it tends to be the heterogametic sex. This pattern is considered a fundamental law of speciation, and is known to be caused by several separate mechanisms. One such mechanism may be the divergence at loci affecting sex chromosome meiotic drive. Cyrtodiopsis dalmanni and C. whitei are sister species of stalk-eyed fly found in Southeast Asia and in which a sizable proportion of wild-caught males produce female-biased broods due to X chromosome meiotic drive. I cross multiple populations of these two species and use QTL mapping and DNA sequencing techniques to test three predictions of the meiotic drive hypothesis of Haldane's rule. In chapter 1, my results show that male hybrid sterility is the fastest-evolving form of reproductive isolation in these species, consistent with Haldane's rule. In chapter 2, I show that DNA sequence evolution is consistent with a pattern of repeated selective sweeps associated with X-linked meiotic drive. In chapter 3, I report the discovery of autosomal suppressors of drive, a Y-linked suppressor, a cryptic (suppressed) driver, an inviability effect of drive, and several QTL for sterility and one QTL for male-biased progeny sex ratios. The suppressors and cryptic driver support the conclusion, from chapter 2, that meiotic drive and suppressors have evolved repeatedly in response to each other. The sterility and sex ratio QTL did not map to the same genetic marker interval, which is not necessarily inconsistent with the drive hypothesis if sufficient time has elapsed to allow additional sterility loci to evolve. Overall, these results provide several lines of support for the meiotic drive hypothesis of Haldane's rule, which is rapidly gaining traction among researchers in the field of speciation. This conclusion suggests that attempts should be made to identify specific genes affecting meiotic drive and male hybrid sterility in Cyrtodiopsis.