Autosomal suppression and fitness costs of an old driving X chromosome in Drosophila testacea.

Driving X chromosomes (X 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 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 was recently discovered in the mycophagous fly, Drosophila testacea, presenting the opportunity to compare this X with the well-studied X of its sister species, Drosophila neotestacea. Comparing features of independently evolved X s in young sister species is a promising avenue towards understanding how X s and their counteracting forces change over time. In contrast to the X of D. neotestacea, we find that the X 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 s should be more deleterious to carriers, we assessed the effect of the X 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 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 male fertility is lower under sperm-depleting conditions, X 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 evolution where the dynamics of young X s are governed by fitness consequences in males, whereas in older X systems, both suppression and fitness consequences in females likely supersede male fitness costs.