Maleness-on-the-Y ( MoY ) orchestrates male sex determination in major agricultural fruit fly pests

Abstract

In insects, rapidly evolving primary sex-determining signals are transduced by a conserved regulatory module controlling sexual differentiation. In the agricultural pest Ceratitis capitata (Mediterranean fruit fly, or Medfly), we identified a Y-linked gene, Maleness-on-the-Y (MoY), encoding a small protein that is necessary and sufficient for male development. Silencing or disruption of MoY in XY embryos causes feminization, whereas overexpression of MoY in XX embryos induces masculinization. Crosses between transformed XY females and XX males give rise to males and females, indicating that a Y chromosome can be transmitted by XY females. MoY is Y-linked and functionally conserved in other species of the Tephritidae family, highlighting its potential to serve as a tool for developing more effective control strategies against these major agricultural insect pests.

Evolution of Sex Determination and Sex Chromosomes: A Novel Alternative Paradigm

“…[ 4,7,22,61,62 ] Advances in molecular biology and genomics have improved our ability to characterize sex chromosomes, sex determining genes, and sex chromosome turnovers across animal taxa. [ 29,36,63–67 ] This work has largely confirmed that sex chromosome turnovers occur via the canonical trajectories described above (Figure 1A–C). For example, a sex chromosome turnover was identified in the lineage leading to Drosophila —an autosome was converted into a sex chromosome, and the ancestral X chromosome reverted to an autosome.…”

“…In most flies, a Y‐linked male‐determiner regulates the splicing of the autosomal tra gene, which then regulates the splicing of downstream genes in the sex determination pathway. [ 35,36 ] However, a dominant allele of tra ( Md‐tra D ) exists in some house fly populations; Md‐tra D is a female‐determiner that is resistant to regulation by the male‐determining gene. [ 29,37 ] The autosome carrying Md‐tra D has thus been converted into a proto‐W chromosome, but this is still segregating as a polymorphism in natural populations.…”

“…The ancestral fly karyotype contains a gene‐poor X chromosome, known as Muller element F. [ 32 ] In many fly species, this X chromosome is paired with a Y chromosome that carries a male‐determining gene. [ 35,36 ] Element F is an X chromosome in many house fly populations, but other chromosomes can also be sex‐linked. [ 38 ] This is because the house fly has a new male‐determining gene ( Mdmd ) that transposed onto multiple different chromosomes, [ 29 ] and each chromosome carrying Mdmd is a proto‐Y.…”

The X chromosome of the German cockroach, Blattella germanica, is homologous to a fly X chromosome despite 400 million years divergence

“…In the female, there is not a significant difference in heterozygosity between genes assigned to element F and genes on the other five elements (P =0. 32 in both sexes has a value of 0.5. Of the 40 element F homologs with sequencing coverage and heterozygosity data, 10 (25%) have both log 2 M F < −0.5 and fraction of male heterozygous variants < 0.5 ( Figure 3C).…”

“…It is most parsimonious to conclude that the ancestral sex determination system of brachyceran dipterans (which includes flies but excludes mosquitoes, craneflies, midges, gnats, etc.) consists of a Y-linked male-determining factor that regulates the splicing of the transformer (tra) gene product [15,20,24,[29][30][31][32]. The ancestral male-determining gene of brachyceran flies is yet to be identified, if it is even still present in any extant species.…”