Germline restricted chromosomes in dark winged fungus gnats show dynamic chromosome organisation despite strong purifying selection on genes

Abstract

Germline restricted chromosomes (GRCs) are an evolutionary mystery. While they seem to be important and perhaps indispensable in species they occur, they also show surprising variability in copy number and size. We are just beginning to understand the evolutionary significance of these chromosomes. One factor that impedes our understanding is that at present, few clades with these chromosomes have been studied in depth. We genomically investigate the GRCs in dark-winged fungus gnats (Sciaridae), a cosmopolitan and species-rich taxa which have harboured GRCs for at least 58 million years. Sciaridae species carry from 1-4 large GRCs which evolved through introgression from the Cecidomyiidae lineage. We produce the first male germline chromosome-scale genome assemblies for the sciarids Bradysia coprophila, B. impatiens, and Lycoriella ingenua. Comparing the GRCs both between and within species, we find that these chromosomes evolve in an extraordinarily dynamic fashion, with very little conservation of synteny or gene content. Puzzlingly, despite this variability, GRCs are gene rich and their genes are evolving under strong purifying selection. Additionally, we uncover evidence that somatic elimination of GRCs potentially occurs via a satellite mediated process. Our study sheds light on the mechanisms of meiosis, tissue restriction, chromosome elimination, and gives us a better appreciation for the diversity of genetic systems that not only persist, but thrive in nature. Significance statementGermline restricted chromosomes (GRCs) are a fascinating evolutionary puzzle. They are restricted to the germline early in development, have unusual transmission dynamics and are more variable than core chromosomes, but also seem to be indispensable in clades they occur in. We generate chromosome level GRC assemblies from three species of fungus gnats (Sciaridae, Diptera). We find that the GRCs, which originated via a cross-family hybridization event, are evolving much more dynamically than other chromosomes in the genome. The five GRCs we sequence are all large, gene-rich, and seem to carry functional genes, but contain mostly a non-overlapping gene set, suggesting that four of the five GRCs we sequenced did not evolve from the same original chromosome.