Avian germline-restricted chromosomes are reservoirs for active and expressed long-terminal-repeat retroviruses

Germline-restricted chromosomes (GRCs) occur only in germ cells and are absent from somatic cells in songbirds, but their contents and evolutionary mechanisms remain poorly understood. We performed comparative genomics on long-read GRC assemblies from male house finch (HF) (Haemorhous mexicanus), common rosefinch (RF) (Carpodacus erythrinus), and blue tit (Cyanistes caeruleus), the first two of which are newly assembled and annotated. The assemblies vary widely in size (6.5-168.4 Mb) and gene content; whereas most GRC-linked genes are species specific, a small conserved set predates the diversification of passerine birds 47 mya. Despite genic variability, GRCs are consistently repeat rich (63.7%-79.5%) and accumulate intact endogenous retroviruses (ERVs) with long terminal repeats (LTRs). This ERV proliferation peaked during the passerine radiation. In contrast, regular chromosomes purge ERVs to generate solo LTRs. Transcriptomic data reveal significantly higher ERV transcription on GRCs than on regular chromosomes in HF testis. We propose that GRCs act as reservoirs of active ERVs, potentially promoting germline transposition and accelerating speciation.