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.

Sexual reproduction is ubiquitous in eukaryotes, but the mechanisms by which sex is determined are diverse and undergo rapid turnovers in short evolutionary timescales. Usually, an embryo’s sex is fated at the moment of fertilisation, but in rare instances it is the maternal genotype that determines the offspring’s sex. These systems are often characterised by mothers producing single-sex broods, a phenomenon known as monogeny. Monogenic reproduction is well documented in Hymenoptera (ants, bees and wasps), where it is associated with a eusocial lifestyle. However, it is also known to occur in three families in Diptera (true flies): Sciaridae, Cecidomyiidae and Calliphoridae. Here we review current knowledge of monogenic reproduction in these dipteran clades. We discuss how this strange reproductive strategy might evolve, and we consider the potential contributions of inbreeding, sex ratio distorters, and polygenic control of the sex ratio. Finally, we provide suggestions on future work to elucidate the origins of this unusual reproductive strategy. We propose that studying these systems will contribute to our understanding of the evolution and turnover of sex determination systems.

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 (&lt;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.