The Potential for a Released Autosomal X-Shredder Becoming a Driving-Y Chromosome and Invasively Suppressing Wild Populations of Malaria Mosquitoes

Sex-ratio distorters based on X-chromosome shredding are more efficient than sterile male releases for population suppression. X-shredding is a form of sex distortion that skews spermatogenesis of XY males towards the preferential transmission of Y-bearing gametes, resulting in a higher fraction of...

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Autores principales:	Yehonatan Alcalay, Silke Fuchs, Roberto Galizi, Federica Bernardini, Roya Elaine Haghighat-Khah, Douglas B. Rusch, Jeffrey R. Adrion, Matthew W. Hahn, Pablo Tortosa, Rachel Rotenberry, Philippos Aris Papathanos
Formato:	article
Lenguaje:	EN
Publicado:	Frontiers Media S.A. 2021
Materias:	gene drive malaria sex-ratio distortion genetic control risk assessment Biotechnology TP248.13-248.65
Acceso en línea:	https://doaj.org/article/a6b4faa8d2fc436aa5fb62f07c00713e
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spelling	oai:doaj.org-article:a6b4faa8d2fc436aa5fb62f07c00713e2021-12-03T06:29:44ZThe Potential for a Released Autosomal X-Shredder Becoming a Driving-Y Chromosome and Invasively Suppressing Wild Populations of Malaria Mosquitoes2296-418510.3389/fbioe.2021.752253https://doaj.org/article/a6b4faa8d2fc436aa5fb62f07c00713e2021-12-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fbioe.2021.752253/fullhttps://doaj.org/toc/2296-4185Sex-ratio distorters based on X-chromosome shredding are more efficient than sterile male releases for population suppression. X-shredding is a form of sex distortion that skews spermatogenesis of XY males towards the preferential transmission of Y-bearing gametes, resulting in a higher fraction of sons than daughters. Strains harboring X-shredders on autosomes were first developed in the malaria mosquito Anopheles gambiae, resulting in strong sex-ratio distortion. Since autosomal X-shredders are transmitted in a Mendelian fashion and can be selected against, their frequency in the population declines once releases are halted. However, unintended transfer of X-shredders to the Y-chromosome could produce an invasive meiotic drive element, that benefits from its biased transmission to the predominant male-biased offspring and its effective shielding from female negative selection. Indeed, linkage to the Y-chromosome of an active X-shredder instigated the development of the nuclease-based X-shredding system. Here, we analyze mechanisms whereby an autosomal X-shredder could become unintentionally Y-linked after release by evaluating the stability of an established X-shredder strain that is being considered for release, exploring its potential for remobilization in laboratory and wild-type genomes of An. gambiae and provide data regarding expression on the mosquito Y-chromosome. Our data suggest that an invasive X-shredder resulting from a post-release movement of such autosomal transgenes onto the Y-chromosome is unlikely.Yehonatan AlcalaySilke FuchsRoberto GaliziFederica BernardiniRoya Elaine Haghighat-KhahDouglas B. RuschJeffrey R. AdrionMatthew W. HahnMatthew W. HahnPablo TortosaRachel RotenberryPhilippos Aris PapathanosFrontiers Media S.A.articlegene drivemalariasex-ratio distortiongenetic controlrisk assessmentBiotechnologyTP248.13-248.65ENFrontiers in Bioengineering and Biotechnology, Vol 9 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	gene drive malaria sex-ratio distortion genetic control risk assessment Biotechnology TP248.13-248.65
spellingShingle	gene drive malaria sex-ratio distortion genetic control risk assessment Biotechnology TP248.13-248.65 Yehonatan Alcalay Silke Fuchs Roberto Galizi Federica Bernardini Roya Elaine Haghighat-Khah Douglas B. Rusch Jeffrey R. Adrion Matthew W. Hahn Matthew W. Hahn Pablo Tortosa Rachel Rotenberry Philippos Aris Papathanos The Potential for a Released Autosomal X-Shredder Becoming a Driving-Y Chromosome and Invasively Suppressing Wild Populations of Malaria Mosquitoes
description	Sex-ratio distorters based on X-chromosome shredding are more efficient than sterile male releases for population suppression. X-shredding is a form of sex distortion that skews spermatogenesis of XY males towards the preferential transmission of Y-bearing gametes, resulting in a higher fraction of sons than daughters. Strains harboring X-shredders on autosomes were first developed in the malaria mosquito Anopheles gambiae, resulting in strong sex-ratio distortion. Since autosomal X-shredders are transmitted in a Mendelian fashion and can be selected against, their frequency in the population declines once releases are halted. However, unintended transfer of X-shredders to the Y-chromosome could produce an invasive meiotic drive element, that benefits from its biased transmission to the predominant male-biased offspring and its effective shielding from female negative selection. Indeed, linkage to the Y-chromosome of an active X-shredder instigated the development of the nuclease-based X-shredding system. Here, we analyze mechanisms whereby an autosomal X-shredder could become unintentionally Y-linked after release by evaluating the stability of an established X-shredder strain that is being considered for release, exploring its potential for remobilization in laboratory and wild-type genomes of An. gambiae and provide data regarding expression on the mosquito Y-chromosome. Our data suggest that an invasive X-shredder resulting from a post-release movement of such autosomal transgenes onto the Y-chromosome is unlikely.
format	article
author	Yehonatan Alcalay Silke Fuchs Roberto Galizi Federica Bernardini Roya Elaine Haghighat-Khah Douglas B. Rusch Jeffrey R. Adrion Matthew W. Hahn Matthew W. Hahn Pablo Tortosa Rachel Rotenberry Philippos Aris Papathanos
author_facet	Yehonatan Alcalay Silke Fuchs Roberto Galizi Federica Bernardini Roya Elaine Haghighat-Khah Douglas B. Rusch Jeffrey R. Adrion Matthew W. Hahn Matthew W. Hahn Pablo Tortosa Rachel Rotenberry Philippos Aris Papathanos
author_sort	Yehonatan Alcalay
title	The Potential for a Released Autosomal X-Shredder Becoming a Driving-Y Chromosome and Invasively Suppressing Wild Populations of Malaria Mosquitoes
title_short	The Potential for a Released Autosomal X-Shredder Becoming a Driving-Y Chromosome and Invasively Suppressing Wild Populations of Malaria Mosquitoes
title_full	The Potential for a Released Autosomal X-Shredder Becoming a Driving-Y Chromosome and Invasively Suppressing Wild Populations of Malaria Mosquitoes
title_fullStr	The Potential for a Released Autosomal X-Shredder Becoming a Driving-Y Chromosome and Invasively Suppressing Wild Populations of Malaria Mosquitoes
title_full_unstemmed	The Potential for a Released Autosomal X-Shredder Becoming a Driving-Y Chromosome and Invasively Suppressing Wild Populations of Malaria Mosquitoes
title_sort	potential for a released autosomal x-shredder becoming a driving-y chromosome and invasively suppressing wild populations of malaria mosquitoes
publisher	Frontiers Media S.A.
publishDate	2021
url	https://doaj.org/article/a6b4faa8d2fc436aa5fb62f07c00713e
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The Potential for a Released Autosomal X-Shredder Becoming a Driving-Y Chromosome and Invasively Suppressing Wild Populations of Malaria Mosquitoes

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