Analysis of new retrogenes provides insight into dog adaptive evolution

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.

The de novo assembly of a European wild boar genome revealed unique patterns of chromosomal structural variations and segmental duplications

“…Gene duplications can be roughly classified into two types, RNA-and DNA-mediated gene duplications, with the former arising through a mechanism termed retroposition or retroduplication (Kaessmann et al, 2009), whereas the latter is processed by several mechanisms, including unequal cross-over and tandem, segmental, chromosomal and genome duplications (Kozlov, 2014). Previous reports have revealed the inter-chromosomal events of retrogenes (RNA-mediated gene duplications) in human, mouse, domestic pig and dog, and have found that X-derived retrogenes in autosomes are excessive (Betrán et al, 2002;Chen et al, 2019;Gao et al, 2019). There are also findings on the excess of X-derived genes on autosomes based on evidence of DNA-mediated gene duplication (Vibranovski et al, 2009).…”

Recent, full-length gene retrocopies are common in canids

“…Previous analyses of canid retrocopies have focused on those retrocopies present in the CanFam3.1 reference assembly, which was produced from a single dog ( Hoeppner et al 2014 ; Rosikiewicz et al 2017 ; Gao et al 2019 ). In this study, we characterized a rich landscape of retroCNVs in canids, consistent with an active LINE-1.…”

“…Estimates of gene retrotransposition rates have varied, although recent analyses using high-coverage WGS data have identified 1663 retroCNV parent genes in populations of mice ( Zhang et al 2021 ) and 503 in human populations ( Zhang et al 2017 ), indicating that gene retrotransposition is a common occurrence. There is limited information about retroCNVs in dogs ( Gao et al 2019 ; Kim et al 2019 ; Batcher et al 2020 ); however, short interspersed nuclear element (SINE) insertions, which are also mobilized in trans by LINE-1 encoded proteins in a manner similar to gene retrocopies, have been shown to be highly dimorphic in dogs ( Wang and Kirkness 2005 ; Halo et al 2021 ).…”

Duplications and retrogenes are numerous and widespread in modern canine genomic assemblies

“…In total, only eleven genes share the top ten spots across all assemblies. Most of the top annotated genes identifies known retrocopy producers in human and/or canine (GAPDH, HNRNPA1, EEF1A1, HMGN2 and the RPL genes) [56][57][58][59][60]. Across all nine assemblies, an average of 859.7 retrocopies retain both hallmarks (32.4%).…”