Search

Gene regulation in the germline ensures the production of high-quality gametes, long-term maintenance of the species and speciation. Male germline transcriptomes undergo dynamic changes after the mitosis-to-meiosis transition and have been subject to evolutionary divergence among mammals. However, the mechanisms underlying germline regulatory divergence remain undetermined. Here, we show that endogenous retroviruses (ERVs) influence species-specific germline transcriptomes. After the mitosis-to-meiosis transition in male mice, specific ERVs function as active enhancers to drive germline genes, including a mouse-specific gene set, and bear binding motifs for critical regulators of spermatogenesis, such as A-MYB. This raises the possibility that a genome-wide transposition of ERVs rewired germline gene expression in a species-specific manner. Of note, independently evolved ERVs are associated with the expression of human-specific germline genes, demonstrating the prevalence of ERV-driven mechanisms in mammals. Together, we propose that ERVs fine-tune species-specific transcriptomes in the mammalian germline.

Gene regulation in the germline ensures the production of high-quality gametes, long-term maintenance of the species and speciation. Male germline transcriptomes undergo dynamic changes after the mitosis-to-meiosis transition and have been subject to evolutionary divergence among mammals. However, the mechanisms underlying germline regulatory divergence remain undetermined. Here, we show that endogenous retroviruses (ERVs) influence species-specific germline transcriptomes. After the mitosis-to-meiosis transition in male mice, specific ERVs function as active enhancers to drive germline genes, including a mouse-specific gene set, and bear binding motifs for critical regulators of spermatogenesis, such as A-MYB. This raises the possibility that a genome-wide transposition of ERVs rewired germline gene expression in a species-specific manner. Of note, independently evolved ERVs are associated with the expression of human-specific germline genes, demonstrating the prevalence of ERV-driven mechanisms in mammals. Together, we propose that ERVs fine-tune species-specific transcriptomes in the mammalian germline.

In birds, the noncoding control region (CR) and its flanking genes are the only parts of the mitochondrial (mt) genome that have been modified by intragenomic rearrangements. In raptors, two noncoding regions are present: the CR has shifted to a new position with respect to the ‘‘ancestral avian gene order,’’ whereas the pseudo-control region (CCR) is located at the original genomic position of the CR. As possible mechanisms for this rearrangement, duplication and transposition have been considered. During characterization of the mt gene order in Bonelli’s eagle Hieraaetus fasciatus, we detected intragenomic sequence similarity between the two regions supporting the duplication hypothesis. We performed intra- and intergenomic sequence comparisons in H. fasciatus and other falconiform species to trace the evolution of the noncoding mtDNA regions in Falconiformes. We identified sections displaying different levels of similarity between the CR and CCR. On the basis of phylogenetic analyses, we outline an evolutionary scenario of the underlying mutation events involving duplication and homogenization processes followed by sporadic deletions. Apparently, homogenization may easily occur if sufficient sequence similarity between the CR and CCR exists. Moreover, homogenization itself allows perpetuation of this continued equalization, unless this process is stopped by deletion. The Pandionidae and the Aquilinae seem to be the only two lineages of Falconiformes where homology between both regions is still detectable, whereas in other raptors no similarity was found so far. In these two lineages, the process of sequence degeneration may have slowed down by homogenization events retaining high sequence similarity at least in some sections.