Accelerated adaptive evolution on a newly formed X chromosome

Abstract

Sex chromosomes originated from ordinary autosomes, and their evolution is characterized by continuous gene loss from the ancestral Y chromosome. Here, we document a new feature of sex chromosome evolution: bursts of adaptive fixations on a newly formed X chromosome. Taking advantage of the recently formed neo-X chromosome of Drosophila miranda, we compare patterns of DNA sequence variation at genes located on the neo-X to genes on the ancestral X chromosome. This contrast allows us to draw inferences of selection on a newly formed X chromosome relative to background levels of adaptation in the genome while controlling for demographic effects. Chromosome-wide synonymous diversity on the neo-X is reduced 2-fold relative to the ancestral X, as expected under recent and recurrent directional selection. Several statistical tests employing various features of the data consistently identify 10%-15% of neo-X genes as targets of recent adaptive evolution but only 1%-3% of genes on the ancestral X. In addition, both the rate of adaptation and the fitness effects of adaptive substitutions are estimated to be roughly an order of magnitude higher for neo-X genes relative to genes on the ancestral X. Thus, newly formed X chromosomes are not passive players in the evolutionary process of sex chromosome differentiation, but respond adaptively to both their sex-biased transmission and to Y chromosome degeneration, possibly through demasculinization of their gene content and the evolution of dosage compensation.

Figure 1. Karyotype of Drosophila miranda

The ancestral X chromosome consists of two chromosomal arms; X-L (light grey), which is part of the X chromosome in all species of the genus Drosophila (>60 MY old), and X-R (medium grey), a former autosome that fused to X-L approximately 10 MY ago. The neo-sex chromosomes (dark grey) were formed by the fusion of another autosome to the ancestral Y chromosome about 1 MY ago. The neo-X chromosome segregates with the X chromosome in D. miranda, but is not fused to it. X-R has already acquired all the stereotypical properties of X chromosomes, whereas the neo-sex chromosomes are in transition from an ordinary autosome to a pair of heteromorphic sex chromosomes.

Figure 2. The Maximized Composite Likelihood Surface Calculated for Genes from the Ancestral X and the Neo-X Chromosome

The horizontal line indicates the 5% cutoff values (LR_crit) as determined separately for the X (LR_crit = 4.5) and the neo-X (LR_crit = 2.7) by simulation under a neutral equilibrium model. More significant peaks are identified on the neo-X, suggesting that more recent selective sweeps have occurred on this chromosome.

Figure 3. Approximate Bayesian Estimation of the Rate of Adaptive Substitutions (2N_eλ) and Their Average Effect on Fitness (s) for Genes from the Ancestral X and the Neo-X Chromosome

Estimation is based on 10⁶ draws from the prior (s ∼ Uniform (1.0E−06, 1.0) and 2N_eλ ∼ Uniform (1.0E−07, 1.0E−01)). (Top) The joint posterior distributions for the X and neo-X. The dotted lines correspond to MAP estimates, and darker regions indicate greater posterior density. (Bottom) The marginal posterior distributions for the strength and rate of sweeps. The marginal posterior distribution for the X is indicated in grey, and for the neo-X in black. Both the rate and the strength of selection are inferred to be an order of magnitude higher for neo-X–linked genes.