High rate of sex chromosome turnover in muscid flies

Authors: MEISEL, RICHARD - UNIVERSITY OF HOUSTON; Olafson, Pia; GUERRERO, FELICITO; KONGANTI, KRANTI - TEXAS A&M UNIVERSITY; BENOIT, JOSHUA - UNIVERSITY OF CINCINNATI

Submitted to: G3, Genes/Genomes/Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/10/2020
Publication Date: 4/1/2020
Citation: Meisel, R.P., Olafson, P.U., Guerrero, F., Konganti, K., Benoit, J.B. 2020. High rate of sex chromosome turnover in muscid flies. G3, Genes/Genomes/Genetics. 10(4):1341-1352. https://doi.org/10.1534/g3.119.400923.
DOI: https://doi.org/10.1534/g3.119.400923

Interpretive Summary: Sex chromosomes and the genes that determine the eventual sex of a developing organism can experience a high rate of evolutionary change Although a substantial body of population genetics theory has been developed and tested to explain this rapid evolution, we do not know why the rates of sex chromosome turnover di'er among different species. Addressing this question will require comparing closely related taxa with fast and slow rates of sex chromosome change to identify biological features that could explain these rate di'erences. Muscid 'ies (e.g., house 'y,horn fly, and stable fly) and blow 'ies appear to have the necessary traits for these studies. There appear to be multiple sex chromosome change events amongst muscids and very few in blow 'ies. However, we do not know the extent to which muscid sex chromosomes are independently derived along di'erent evolutionary lineages. To address that question, we used genomic sequence data to identify young sex chromosomes in two closely related muscid 'y species, horn 'y (Haematobia irritans) and stable 'y (Stomoxys calcitrans). We provide evidence that the nascent sex chromosomes of horn 'y and stable 'y were derived independently from each other and from the young sex chromosomes of the closely related house 'y (Musca domestica). We present three di'erent scenarios that could have given rise to the sex chromosomes of horn 'y and stable 'y, and we describe how the scenarios could be distinguished. Distinguishing between these scenarios in future work could help to identify features of muscid genomes that promote sex chromosome turnover.

Technical Abstract: Sex chromosomes and the sex determining genes that reside on them can experience a high rate of evolutionary turnover in some taxa and evolutionary lineages. A substantial body of population genetics theory has been developed and tested to explain this rapid evolution. In contrast, we do not know why the rates of sex chromosome turnover di'er across taxa. Addressing this question will require comparing closely related taxa with fast and slow rates of sex chromosome turnover to identify biological features that could explain these rate di'erences. Cytological karyotypes suggest that muscid 'ies (e.g., house 'y) and blow 'ies are such a taxonomic pair. There appear to be multiple sex chromosome turnover events amongst muscids and very few in blow 'ies. However, we do not know the extent to which muscid sex chromosomes are independently derived along di'erent evolutionary lineages. To address that question, we used genomic data to identify young sex chromosomes in two closely related muscid 'y species, horn 'y (Haematobia irritans) and stable 'y (Stomoxys calcitrans). We provide evidence that the nascent sex chromosomes of horn 'y and stable 'y were derived independently from each other and from the young sex chromosomes of the closely related house 'y (Musca domestica). We present three di'erent scenarios that could have given rise to the sex chromosomes of horn 'y and stable 'y, and we describe how the scenarios could be distinguished. Distinguishing between these scenarios in future work could help to identify features of muscid genomes that promote sex chromosome turnover.