Recent evolution of a maternally-acting sex-determining supergene in a fly with single-sex broods

Abstract

Sex determination is a key developmental process, yet it is remarkably variable across the tree of life. The dipteran family Sciaridae exhibits one of the most unusual sex determination systems in which mothers control offspring sex through selective elimination of paternal X chromosomes. Whereas in some members of the family females produce mixed-sex broods, others such as the dark-winged fungus gnat Bradysia coprophila are monogenic, with females producing single-sex broods. Female-producing females were previously found to be heterozygous for a large X-linked paracentric inversion (X'), which is maternally inherited and absent from male-producing females. Here we assembled and characterized the X' sequence. As close sequence homology between the X and X' made identification of the inversion challenging, we developed a k-mer-based approach to bin genomic reads before assembly. We confirmed that the inversion spans most of the X' chromosome (approximately 55Mb) and encodes around 3500 genes. Analysis of the divergence between the inversion and the homologous region of the X revealed that it originated very recently (<0.5 mya). Surprisingly, we found that the X' is more complex than previously thought and is likely to have undergone multiple rearrangements that have produced regions of varying ages, resembling a supergene composed of evolutionary strata. We found functional degradation of around 7.3% of genes within the region of recombination suppression, but no evidence of accumulation of repetitive elements. Our findings provide an indication that sex-linked inversions are driving turnover of the strange sex determination system in this family of flies.

Parthenogenesis in dipterans: a genetic perspective

“…However, there is little mechanistic understanding of how chromosome elimination occurs and how parthenogenesis might alter this process. Gall midges are not the only family that undergo chromosome elimination, the fungus gnat family are able to select the sex of their offspring through sex chromosome elimination [ 38 ].…”

Laboratory Maintenance of the Lower Dipteran Fly <em>Bradysia (Sciara) coprophila</em>: A New/Old Emerging Model Organism

“…Females that have the X' ("X-prime") chromosome with a long paracentric inversion will have only daughters, whereas females that are homozygous for the standard (non-inverted) X chromosome will have only sons 5 (Figure 2). Sequence information is available for the X' chromosome 19 , but the molecular mechanism remains to be elucidated on how the X' chromosome determines that offspring will be females. Males never have the X' chromosome, and after fertilization, females are X'X (heterozygous for the X') or XX.…”

JoVE Video Dataset

“…Females that have the X' ("X-prime") chromosome with a long paracentric inversion will have only daughters, whereas females that are homozygous for the standard (non-inverted) X chromosome will have only sons 5 (Figure 2). Sequence information is available for the X' chromosome 19 , but the molecular mechanism remains to be elucidated on how the X' chromosome determines that offspring will be females. Males never have the X' chromosome, and after fertilization, females are X'X (heterozygous for the X') or XX.…”