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MBE Advance Access originally published online on July 23, 2007
Molecular Biology and Evolution 2007 24(10):2242-2253; doi:10.1093/molbev/msm153
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© The Author 2007. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org

Research Articles

Origins of New Male Germ-line Functions from X-Derived Autosomal Retrogenes in the Mouse

Meng-Shin Shiao*,{dagger}, Pavel Khil{ddagger}, R. Daniel Camerini-Otero{ddagger}, Toshihiko Shiroishi§, Kazuo Moriwaki||, Hon-Tsen Yu{dagger} and Manyuan Long*

* Department of Ecology and Evolution, University of Chicago
{dagger} Institute of Zoology, National Taiwan University, Taipei, Taiwan
{ddagger} Genetics and Biochemistry Branch, National Institute of Diabetes and Digestive and Kidney Disease, National Institutes of Health, Bethesda, MD
§ National Institute of Genetics, Mishima, Shizuoka-ken, Japan
|| RIKEN BioResources Center, Tsukuba-shi, Ibaraki, Japan
Department of Life Science, National Taiwan University, Taipei, Taiwan

E-mail: mlong{at}uchicago.edu; ayu{at}ntu.edu.tw.

Accepted for publication July 16, 2007.

Recent literature demonstrates that retrogenes tend to leave the X chromosome and integrate onto the autosomes and evolve male-biased expression patterns. Several selection-based evolutionary mechanisms have been proposed to explain this observation. Testing these selection-based models requires examining the evolutionary history and functional properties of new retrogenes, particularly those that show evidence of directional movement between the X and the autosomes (X-related retrogenes). This includes autosomal retrogenes with parental paralogs on the X chromosome (X-derived autosomal retrogenes) and those retrogenes integrated onto the X chromosomes (X-linked retrogenes). In order to understand why retrogenes tend to move nonrandomly in genomes, we examined the expression patterns and evolutionary mechanisms concerning gene pairs having young retrogenes—originating less than 20 MYA (after mouse–rat split). We demonstrate that these X-derived autosomal retrogenes evolved a more restricted male-biased expression pattern: they are expressed exclusively or predominantly in the testis, in particular, during the late stages of spermatogenesis. In contrast, the parental counterparts have relatively broad expression patterns in various tissues and spermatogenetic stages. We further observed that positive selection is targeting these X-derived autosomal retrogenes with novel male-biased expression patterns. This suggests that such retrogenes evolved new male germ-line functions that may be complementary to the functions of the parental paralogs, which themselves contribute little during spermatogenesis. Such evolutionary changes may be beneficial to the populations. Furthermore, most identified X-related retrogenes have recruited novel adjacent sequences as their untranslated regions (UTRs), suggesting that these UTRs, acquired de novo, may play an important role in establishing new regulatory mechanisms to carry out the new male germ-line functions.

Key Words: mouse • retroposition • spermatogenesis • male functions


Takashi Gojobori, Associate Editor


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