Adaptive expansion of ERVK solo-LTRs is associated with Passeriformes speciation events

Guangji Chen, Dan Yu, Yu Yang, Xiang Li, Xiaojing Wang, Danyang Sun, Yanlin Lu, Rongqin Ke, Guojie Zhang, Jie Cui () and Shaohong Feng ()
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Guangji Chen: University of Chinese Academy of Sciences
Dan Yu: Zhejiang University School of Medicine
Yu Yang: Huaqiao University
Xiang Li: Chinese Academy of Sciences
Xiaojing Wang: Chinese Academy of Sciences
Danyang Sun: Zhejiang University School of Medicine
Yanlin Lu: Zhejiang University School of Medicine
Rongqin Ke: Huaqiao University
Guojie Zhang: Zhejiang University School of Medicine
Jie Cui: Fudan University
Shaohong Feng: Zhejiang University School of Medicine

Nature Communications, 2024, vol. 15, issue 1, 1-12

Abstract: Abstract Endogenous retroviruses (ERVs) are ancient retroviral remnants integrated in host genomes, and commonly deleted through unequal homologous recombination, leaving solitary long terminal repeats (solo-LTRs). This study, analysing the genomes of 362 bird species and their reptilian and mammalian outgroups, reveals an unusually higher level of solo-LTRs formation in birds, indicating evolutionary forces might have purged ERVs during evolution. Strikingly in the order Passeriformes, and especially the parvorder Passerida, endogenous retrovirus K (ERVK) solo-LTRs showed bursts of formation and recurrent accumulations coinciding with speciation events over past 22 million years. Moreover, our results indicate that the ongoing expansion of ERVK solo-LTRs in these bird species, marked by high transcriptional activity of ERVK retroviral genes in reproductive organs, caused variation of solo-LTRs between individual zebra finches. We experimentally demonstrated that cis-regulatory activity of recently evolved ERVK solo-LTRs may significantly increase the expression level of ITGA2 in the brain of zebra finches compared to chickens. These findings suggest that ERVK solo-LTRs expansion may introduce novel genomic sequences acting as cis-regulatory elements and contribute to adaptive evolution. Overall, our results underscore that the residual sequences of ancient retroviruses could influence the adaptive diversification of species by regulating host gene expression.

Date: 2024
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DOI: 10.1038/s41467-024-47501-3

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