ScienceDaily (Apr. 25, 2009) — Move over, Y chromosome – it's time X got some attention.
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The neo-X (top) and neo-Y chromosomes of the fruit fly Drosophila miranda, showing how the Y has shrunken slightly through loss of genes. The X has remained about the same size as the fly's other chromosomes, though its genes are in the process of adapting to the Y's degeneration. (Credit: Doris Bachtrog/UC Berkeley)
In the first evolutionary study of the chromosome associated with being female, University of California, Berkeley, biologist Doris Bachtrog and her colleagues show that the history of the X chromosome is every bit as interesting as the much-studied, male-determining Y chromosome, and offers important clues to the origins and benefits of sexual reproduction.
"Contrary to the traditional view of being a passive player, the X chromosome has a very active role in the evolutionary process of sex chromosome differentiation," said Bachtrog, an assistant professor of integrative biology and a member of UC Berkeley's Center for Theoretical Evolutionary Genomics.
Bachtrog, UC Berkeley post-doctoral fellow Jeffrey D. Jensen and former UC San Diego post-doc Zhi Zhang, now at the University of Munich, detail their findings in this week's edition of the open-access journal PLoS Biology.
"In our manuscript, we demonstrate for the first time the flip side of the sex chromosome evolution puzzle: The X chromosome undergoes periods of intense adaptation in the evolutionary process of creating new sections of the genome that govern sexual differentiation in many species, including our own," she said.
Not all animals and plants employ genes to determine if an embryo becomes male or female. Many reptiles, for example, rely on environmental cues such as temperature to specify male or female.
But in life forms that do set aside a pair of chromosomes to specify sex – from fruit flies to mammals and some plants – the two X chromosomes inherited by females look nearly identical to the other non-sex chromosomes, so-called autosomes, Bachtrog said. The Y chromosome, however, which is inherited by males in concert with one X chromosome, is a withered version of the X, having lost many genes since it stopped recombining with the X chromosome.
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Accelerated Adaptive Evolution on a Newly Formed X Chromosome
Doris Bachtrog1*, Jeffrey D. Jensen1, Zhi Zhang2
1 Department of Integrative Biology, University of California, Berkeley, Berkeley, California, United States of America, 2 Division of Biological Sciences, University of California, San Diego, La Jolla, California, United States of America
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.
Funding. JDJ is supported by a National Science Foundation Biological Informatics Postdoctoral Fellowship. This research was funded by National Institutes of Health Grant GM076007, an Alfred P. Sloan Faculty Research Fellowship in Molecular and Computational Biology, and a David and Lucile Packard Foundation Fellowship to DB.
Competing interests. The authors have declared that no competing interests exist.
Academic Editor: Laurence D. Hurst, University of Bath, United Kingdom
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
Received: August 13, 2008; Accepted: February 27, 2009; Published: April 14, 2009
Copyright: © 2009 Bachtrog et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Abbreviations: CLR test, composite likelihood ratio test; GOF test, goodness-of-fit test; HKA test, Hudson-Kreitman-Aguadé test; LD, linkage disequilibrium; MAP, maximum a posteriori; MCLS test, maximized composite likelihood surface test; MY, million years
* To whom correspondence should be addressed. E-mail: dbachtrog@berkeley.edu
AUTHOR SUMMARY
Sex chromosomes have evolved independently many times in both animals and plants from ordinary chromosomes. Much research on sex chromosome evolution has focused on the degeneration and loss of genes from the Y chromosome. Here, we describe another principle of sex chromosome evolution: bursts of adaptive fixations on a newly formed X chromosome. By employing a comparative population genomics approach and taking advantage of the recently formed sex chromosomes in the fruit fly Drosophila miranda, we show that rates of adaptation are increased about 10-fold on a newly formed X chromosome relative to background levels of selection in the genome. This suggests that a young X chromosome responds adaptively to both its female-biased transmission and to Y chromosome degeneration. Thus, contrary to the traditional view of being passive players, the X chromosome has a very active role in the evolutionary process of sex chromosome differentiation.
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