Abstract

The origin and subsequent evolution of new genes have been considered as an important source of genetic and phenotypic diversity in organisms. Dog breeds show great phenotypic diversity for morphological, physiological, and behavioral traits. However, the contributions of newly originated retrogenes, which provide important genetic bases for dog species differentiation and adaptive traits, are largely unknown. Here, we analyzed the dog genome to identify new RNA‐based duplications and comprehensively investigated their origin, evolution, functions in adaptive traits, and gene movement processes. First, we totally identified 3,025 retrocopies including 476 intact retrogenes, 2,518 retropseudogenes, and 31 chimerical retrogenes. Second, selective pressure along with ESTs expression analysis showed that most of the intact retrogenes were significantly under stronger purifying selection and subjected to more functional constraints when compared to retropseudogenes. Furthermore, a large number of retrocopies and chimerical retrogenes that occurred approximately 22 million years ago implied a burst of retrotransposition in the dog genome after the divergence time between dog and its closely related species red fox. Interestingly, GO and pathway analyses showed that new retrogenes had expanded in glutathione biosynthetic/metabolic process which likely provided important genetic basis for dogs' adaptation to scavenge human waste dumps. Finally, consistent with the results in human and mouse, a significant excess of functional retrogenes movement on and off the X chromosome in the dog confirmed a general pattern of gene movement process in mammals which was likely driven by natural selection or sexual antagonism. Together, these results increase our understanding that new retrogenes can reshape the dog genome and provide further exploration of the molecular mechanisms underlying the dogs' adaptive evolution.

Highlights

  • Since the age of Darwin, biologists have been following an essential question: How do organisms evolve from their common ancestor to a rich variety of species? The origin and subsequent evolution of novel genes have been taken into account as a major contributor to adaptive evolution (Kaessmann, 2010)

  • The single coding exon gene was defined as a retrogene while the multiple coding exons gene was defined as its parental gene

  • About 60.6% (285/470) of intact retrogenes had lower ω than 0.5, compared with 39.2% (984/2,509) of retropseudogenes (Table 2). These results indicated that more than half of intact retrogenes were under stronger purifying selection and tended to be subjected to more functional constraints when compared to retropseudogenes

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Summary

| INTRODUCTION

Since the age of Darwin, biologists have been following an essential question: How do organisms evolve from their common ancestor to a rich variety of species? The origin and subsequent evolution of novel genes have been taken into account as a major contributor to adaptive evolution (Kaessmann, 2010). Novel genes provide important genetic novelties associated with biological diversity in organisms (Chen, Krinsky, & Long, 2013) and significantly contribute to the evolution of lineage‐specific or species‐specific phenotypic traits (Chen, Zhang, & Long, 2010). The expression of a newly originated retrogene fibroblast growth factor 4 (fgf4) is strongly associated with chondrodysplasia, a short‐ legged phenotype that defined at least 19 dog breeds which include dachshund, corgi, and basset hound (Parker et al, 2009). These results indicate that a single gene can play critical roles in constraining and directing phenotypic diversity in the dog. If one retrocopy could recruit novel regulatory elements and new protein‐coding exons and evolve into a functional retrogene, it was defined as a chimerical retrogene

| MATERIALS AND METHODS
| RESULTS AND DISCUSSION
| CONCLUSION
CONFLICT OF INTEREST
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