Using a female-specific isoform of doublesex to explore male-specific hearing in mosquitoes

Animal reproduction relies on elaborate divisions of labour and multiple dimorphisms between the sexes. Primary dimorphisms affect core elements of reproduction, secondary dimorphisms affect more indirect traits, including complex behaviours. In disease-transmitting mosquitoes, males locate females acoustically prior to copulation (phonotaxis). No comparable acoustic behaviour is known for females. As a result, the males ears - and hearing performance - have evolved to become substantially more complex. Sex-specific hearing in mosquitoes is in part controlled by the doublesex (dsx) gene. Intriguingly, dsx forms a linker between primary and secondary dimorphisms: spermatogenesis and ear morphogenesis share considerable molecular overlap and both depend on dsx expression patterns. We have combined transcriptomics with functional-anatomical analyses to dissect dsx-dependent hearing in the malaria mosquito Anopheles gambiae. By cross-linking our auditory findings to the genetic bases of spermatogenesis we advance the molecular understanding of sex-specific hearing mechanisms in insects, highlighting the special roles of ciliary factors therein. HighlightsO_LIDisruption of the female-specific exon of the doublesex gene alters hearing in female Anopheles gambiae mosquitoes C_LIO_LIFemale mutant ears are anatomically and functionally distinct from both wild-type male and female; they show a substantial, but incomplete, masculinisation C_LIO_LIContrary to males, and similarly to females, the flagella of female mutants do not exhibit Self-Sustained Oscillations (SSOs) C_LIO_LITranscriptomic comparisons of ears uncovered molecular bases of auditory maleness, these were closely linked to molecular machinery of ciliary function C_LIO_LIComparisons with existing transcriptome from male testes revealed a substantial overlap between male ear and testicular ciliary motility machineries C_LI