Department of Biology, University of Victoria, Victoria, BC, Canada.
Department of Botany, University of British Columbia, Vancouver, BC, Canada.
J Evol Biol. 2020 May;33(5):619-628. doi: 10.1111/jeb.13596. Epub 2020 Feb 24.
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.
X 染色体通过杀死携带 Y 染色体的配子来偏向自身在雄性中的传递。从理论上讲，这些染色体可以在种群中迅速传播并导致灭绝，但许多 X 染色体被发现是平衡的多态性，或者是被驱动抑制物关闭的“隐匿”X 染色体。这些结果的相对可能性以及它们出现的进化途径还不是很清楚。最近在食菌蝇 Drosophila testacea 中发现了一条 X 染色体，这为比较这条 X 染色体与姐妹种 Drosophila neotestacea 的 X 染色体提供了机会。比较年轻姐妹种中独立进化的 X 染色体的特征是理解 X 染色体及其拮抗力量随时间变化的一种很有前途的途径。与 D. neotestacea 的 X 染色体不同，我们发现 D. testacea 的 X 染色体很古老，其起源早于三个物种的辐射：D. testacea、D. neotestacea 及其共同的姐妹种 Drosophila orientacea。鉴于较老的 X 染色体对携带者的危害应该更大的说法，我们评估了 X 染色体对雄性和雌性生育力的影响。与从 D. neotestacea 中所知的情况不同，我们发现 D. testacea 中 X 染色体在纯合雌性中存在强烈的适应度成本：很大一部分纯合雌性在与雄性同居数天后未能产生后代。我们的雄性生育力实验表明，尽管在消耗精子的条件下 X 雄性的生育力较低，但在自由交配条件下，携带 X 染色体的雄性与携带标准 X 染色体的雄性生育力相当，这可能更接近 D. testacea 野生种群的条件。最后，我们证明了常染色体对 X 染色体驱动的抑制作用的存在。我们的结果支持了 X 染色体进化的模型，该模型认为年轻 X 染色体的动态受雄性中适应度后果的控制，而在较老的 X 染色体系统中，雌性的抑制和适应度后果可能超过雄性的适应度成本。
