Evolution of gene-rich germline restricted chromosomes in black-winged fungus gnats through introgression (Diptera: Sciaridae)

Abstract

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 three diverse families, Chironomidae, Cecidomyiidae, and Sciaridae exhibit germline restricted chromosomes (GRCs). We conducted a genomic analysis of germline restricted chromosomes in the fungus gnat Bradysia (Sciara) coprophila (Diptera: Sciaridae), which carries two 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 germ 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 paralogs on other chromosomes in the genome. We also found that the GRC genes are extraordinarily divergent from their paralogs, and have sequence similarity to another Dipteran family (Cecidomyiidae) in phylogenetic analyses, suggesting that these chromosomes have arisen in Sciaridae through introgression from a related lineage. These results suggest that the GRCs may have evolved through an ancient hybridization event, raising questions about how this may have occurred, how these chromosomes became restricted to the germline after introgression, and why they were retained over time.

Evolutionary Perspectives on Germline-Restricted Chromosomes in Flies (Diptera)

“…This theory contains some testable predictions about GRC evolution, namely that they are expected to have evolved after the divergence of Sciaridae from their sister clade (as this family does not exhibit paternal genome elimination) and that they evolved from the X chromosome and therefore would be expected to contain genes derived from this chromosome. However, a recent study found that GRCs in the Sciarid B. coprophila do not bear significant homology to the X chromosome in this species, and instead have homologous regions to all chromosomes in the core genomes, suggesting that in Sciaridae, at least, the GRCs do not seem to have evolved from the X chromosome ( Hodson et al. 2021 ).…”

“…1971 ). Yet, recent genomic evidence suggests that there is likely very little recombination between the two GRCs in B. coprophila ( Hodson et al. 2021 ).…”

“…Further work, however, is needed to characterize the GRCs in this lineage as the experimental design and data quality were insufficient for more in-depth analyses. In the Sciarid B. coprophila , a recent study ( Hodson et al. 2021 ) conducts an in-depth investigation of GRC content.…”

Sexual antagonism in haplodiploids

“…In these groups we may expect female-beneficial variants to be enriched on the autosomes, whilst male-beneficial ones would be expected to be overrepresented on the sex chromosomes, regardless of assumptions about dominance, making this a more straightforward prediction than between autosomes and sex chromosomes in conventional eumendelian systems (Rice 1984; Patten 2019). In addition to X autosome comparisons, some of these groups contain further genomic elements such as germline-restricted chromosomes that are maternally-inherited in gall midges and show paternally-biased inheritance in sciarid flies (Hodson and Ross 2021; Hodson et al 2021), enabling further within-genome comparisons.…”

New Perspectives on the Evolution of Within-Individual Genome Variation and Germline/Soma Distinction

“…Although some insects have numerous GRCs ( Hodson and Ross 2021) and the zebra finch GRC is the largest chromosome of its karyotype ( Pigozzi and Solari 1998) , genomic and transcriptomic data of these GRCs have been restricted to a 19-kb intergenic region of zebra finch GRCs until not so long ago ( Itoh et al 2009) . It is only recently that a wealth of sequencing data has provided first glimpses into the sequence content of GRCs of songbirds (Biederman et al 2018; Kinsella et al 2019; Torgasheva et al 2019; Pei et al 2021) and sciarid flies ( Hodson et al 2021) , revealing that GRCs contain many dozens to hundreds of genes and that they may have existed for millions of years in these lineages (Kinsella et al 2019; Hodson et al 2021) .…”