Autosomal suppression and fitness costs of an old driving X chromosome in Drosophila testacea. (24th February 2020)

• Record Type: Journal Article
• Authors: Keais, Graeme L.; Lu, Sijia; Perlman, Steve J.
• Is Part Of: Journal of evolutionary biology. Volume 33:Number 5(2020)
• Page Start: 619
• Page End: 628
• Publication Date: 2020-02-24
• Subjects: Drosophila -- gamete‐killing -- gene drive -- genetic conflict -- genomic conflict -- meiotic drive -- segregation distortion -- selfish genetic elements -- sex ratio -- X chromosome; Evolution (Biology) -- Periodicals; Biology -- Periodicals; 576.8
• DOI: 10.1111/jeb.13596
• Languages: English
• ISSNs: 1010-061X

Abstract

Abstract: Driving X chromosomes (X D s) bias their own transmission through males by killing Y‐bearing gametes. These chromosomes can in theory spread rapidly in populations and cause extinction, but many are found as balanced polymorphisms or as "cryptic" X D s shut down by drive suppressors. The relative likelihood of these outcomes and the evolutionary pathways through which they come about are not well understood. An X D was recently discovered in the mycophagous fly, Drosophila testacea, presenting the opportunity to compare this X D with the well‐studied X D of its sister species, Drosophila neotestacea . Comparing features of independently evolved X D s in young sister species is a promising avenue towards understanding how X D s and their counteracting forces change over time. In contrast to the X D of D. neotestacea, we find that the X D of D. testacea is old, with its origin predating the radiation of three species: D. testacea, D. neotestacea and their shared sister species, Drosophila orientacea . Motivated by the suggestion that older X D s should be more deleterious to carriers, we assessed the effect of the X D on both male and female fertility. Unlike what is known from D. neotestacea, we found a strong fitness cost in females homozygous for the X D in D. testacea : a large proportion of homozygous females failed to produce offspring after being housed with males for several days. Our male fertility experiments show that although X D male fertility is lower under sperm‐depleting conditions, X D males have comparable fertility to males carrying a standard X chromosome under a free‐mating regime, which may better approximate conditions in wild populations of D. testacea . Lastly, we demonstrate the presence of autosomal suppression of X chromosome drive. Our results provide support for a model of X D evolution where the dynamics of young X D s are governed by fitness consequences in males, whereas in older X D systems, both suppression and fitness consequences in females likely supersede male fitness costs. Abstract : We show that the Drosophila testacea driving X chromosome (XD) is old and highly divergent. We also demonstrate the presence of an autosomal suppressor of X drive, and a considerable reproductive fitness cost in females homozygous for the XD. Male reproductive fitness is also affected by the XD, but only under sperm‐depleting conditions, which may not reflect conditions in the wild.