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The neo-X on the fly

Gene Expression
By Razib Khan
Apr 14, 2009 6:00 PMNov 5, 2019 9:37 AM


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Accelerated Adaptive Evolution on a Newly Formed X Chromosome:

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.

This is an interesting illustration of how the general processes of evolutionary dynamics are constrained and shaped by the specific biophysical nature of genomic architecture. As noted by the authors the Y chromosome tends to undergo a long term evolutionary process of loss of function. This is the foundation of Bryan Sykes' hyperbolic book Adam's Curse: A Future without Men. With the degeneration of the Y chromosome there are many individuals within a population where the X chromosome has to be above reproach, or else the emergence of X-linked recessive pathologies in the heterogametic sex. Additionally the X chromosome "spends" 2/3 of its evolutionary time within female bodies, while the Y chromosome resides exclusively in male bodies. Matt Ridley in The Red Queen: Sex and the Evolution of Human Nature outlines many of the ingenious evolutionary inferences which thinker such as Robert Trivers have made based on these structural parameters. Remember that William D. Hamilton took advantage of the haplodiploid nature of hymenoptera to work out the basics of inclusive fitness in his early seminal papers. In any case in this paper the researchers seem to be catching the genome in a transient state. The nature of chromosomal evolution presumably exhibits more "bursts" than gradualism due to the coarse and discrete nature of this level of genetic organization. Though the initial conditions matter there seems to be a general trend where Y chromosome loses function, the X chromosome evolves in response, and the "battle of the sexes" chromosome style operates in parallel (e.g., genomic imprinting). Despite the exotic circumstance of a new X chromosome being recruited from the autosome, some conventional evolutionary genetics:

...Thus, not only does adaptive evolution appear to be more frequent on a newly formed X chromosome, but also the selective benefit of mutations arising may be larger for genes that have only recently become X-linked relative to genes that have been evolving under a stable chromosomal configuration. This may be expected if genes on a young X chromosome are further away from their optimum fitness...since they experience a new genomic environment (i.e., they used to segregate as an autosome but have only recently become X-linked).

This is just what R. A. Fisher would have expected. Citation: Bachtrog D, Jensen JD, Zhang Z (2009) Accelerated Adaptive Evolution on a Newly Formed X Chromosome. PLoS Biol 7(4): e1000082 doi:10.1371/journal.pbio.1000082

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