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 producing sex-specific proteins that direct sex determination and sexual differentiation 1-4 . In the agricultural pest Ceratitis capitata (medfly), a Y-linked maleness factor (M) is thought to repress the autoregulatory splicing of transformer (Cctra), which is required in XX individuals to establish and maintain female sex determination 5,6 . Despite previous attempts of isolating Y-linked genes using the medfly whole genome, the M factor has remained elusive 7 . Here, we report the identification of a Y-linked gene, Maleness-on the-Y (MoY), and show that it encodes a small novel protein which is both necessary and sufficient for medfly male sex determination. Transient silencing of MoY in XY individuals leads to the development of fertile females while transient expression of MoY in XX individuals results in fertile males. Notably, a cross between these sex reverted individuals gives rise to both fertile males and females indicating that a functional MoY can be maternally transmitted. In contrast to the diversity of M factors found in dipteran species 8-11 , we discovered MoY orthologues in seven other Tephritid species spanning ~111 millions of years of evolution (Mya). We confirmed their male determining function in the olive fly (Bactrocera oleae) and the oriental fruit fly (Bactrocera dorsalis). This unexpected conservation of the primary MoY signal in a large number of important agricultural pests 12will facilitate the development of transferable genetic control strategies in these species, for example sterile male releases or sex-ratio-distorting gene drives.

Sex chromosome evolution in muscid flies

“…The scaffold N50 of the horn fly assembly is 23 Kb (Konganti et al, 2018), and the vast majority (4,112/4,778 = 86%) of horn fly scaffolds assigned to Muller elements have only 1 annotated gene. We also searched for both the house fly and tephritid male-determining genes in the horn fly genome using BLAST (Altschul et al, 1990;Meccariello et al, 2019;Sharma et al, 2017), and we failed to find either.…”

“…All three scenarios assume that the MRCA of muscid flies had a karyotype with five euchromatic autosomes (elements A-E) and a heterochromatic sex chromosome pair (where element F is the X chromosome) because this is the ancestral karyotype of Brachycera Bachtrog, 2013, 2015) and is still conserved in some Muscidae (Fig 1). We additionally assume that the Y chromosome of the MRCA of Muscidae carried a male-determining locus because that is the most common mechanism of sex determination in closely and distantly related families (Bopp et al, 2014;Meccariello et al, 2019;Scott et al, 2014b;Willhoeft and Franz, 1996).…”

“…The house fly maledetermining gene (Mdmd ) was not found in the stable fly genome or any other fly relatives(Sharma et al, 2017). We also searched for the male-determining gene from tephritid flies (MoY ;Meccariello et al, 2019) in the stable fly genome using BLAST(Altschul et al, 1990), and we failed to find anything resembling the MoY protein sequence. Therefore, either stable fly has an independently derived new male-determiner or it has retained an ancestral male-determining locus that was replaced in house fly.The horn fly sex chromosomes consist of elements A and FWe hypothesize that horn fly also has a young X-Y chromosome pair.…”

Genome-wide gene expression profiling of the melon fly, Zeugodacus cucurbitae, during thirteen life stages

“…For example, in Ceratitis capitata, a conserved Maleness-on-the-Y gene was isolated to be involved in the male sex determination by RNA-Seq. 12 . Comprehensive studies of gene expression during various developmental stages in many important insect pests, e.g.…”

Sex Sorting for Pest Control: It’s Raining Men!

“…albopictus [92]. The M-factor in tephritid flies has recently been described and shown to regulate tra's auto-regulatory positive-feedback loop [93]. Similarly, in two phlebotomine sandflies, tra has been recently identified and shown to also be self-regulating [94].…”