Gene-rich germline-restricted chromosomes in black-winged fungus gnats evolved through hybridization

Germline-restricted DNA has evolved in diverse animal taxa and is found in several vertebrate clades, nematodes, and flies. In these lineages, either portions of chromosomes or entire chromosomes are eliminated from somatic cells early in development, restricting portions of the genome to the germline. Little is known about why germline-restricted DNA has evolved, especially in flies, in which 3 diverse families, Chironomidae, Cecidomyiidae, and Sciaridae, carry germline-restricted chromosomes (GRCs). We conducted a genomic analysis of GRCs in the fungus gnat Bradysia (Sciara) coprophila (Diptera: Sciaridae), which has 2 large germline-restricted “L” chromosomes. We sequenced and assembled the genome of B. coprophila and used differences in sequence coverage and k-mer frequency between somatic and germline tissues to identify GRC sequence and compare it to the other chromosomes in the genome. We found that the GRCs in B. coprophila are large, gene rich, and have many genes with divergent homologs on other chromosomes in the genome. We also found that 2 divergent GRCs exist in the population we sequenced. GRC genes are more similar in sequence to genes from another Dipteran family (Cecidomyiidae) than to homologous genes from Sciaridae. This unexpected finding suggests that these chromosomes likely arose in Sciaridae through hybridization with a related lineage. These results provide a foundation from which to answer many questions about the evolution of GRCs in Sciaridae, such as how this hybridization event resulted in GRCs and what features on these chromosomes cause them to be restricted to the germline.

Germ-line restricted chromosomes are eliminated from all somatic tissues while being retained in the germline. This study of the evolutionary origin of such chromosomes in fungus gnats reveals that they are most similar to a fly of a different family, suggesting an ancient allopolyploidization origin for these peculiar chromosomes.