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Genetics. 2017 Oct;207(2):729-740. doi: 10.1534/genetics.117.300221. Epub 2017 Aug 31.

Cross-Species Y Chromosome Function Between Malaria Vectors of the Anopheles gambiae Species Complex.

Author information

1
Department of Life Sciences, Imperial College London, South Kensington Campus, SW7 2AZ, United Kingdom.
2
Malaria Programme, Wellcome Trust Sanger Institute, Hinxton, CB10 1SA Cambridge, United Kingdom.
3
Section of Genomics and Genetics, Department of Experimental Medicine, University of Perugia, 06132, Italy.
4
Department of Life Sciences, Imperial College London, South Kensington Campus, SW7 2AZ, United Kingdom n.windbichler@imperial.ac.uk a.drcrisanti@imperial.ac.uk.

Abstract

Y chromosome function, structure and evolution is poorly understood in many species, including the Anopheles genus of mosquitoes-an emerging model system for studying speciation that also represents the major vectors of malaria. While the Anopheline Y had previously been implicated in male mating behavior, recent data from the Anopheles gambiae complex suggests that, apart from the putative primary sex-determiner, no other genes are conserved on the Y. Studying the functional basis of the evolutionary divergence of the Y chromosome in the gambiae complex is complicated by complete F1 male hybrid sterility. Here, we used an F1 × F0 crossing scheme to overcome a severe bottleneck of male hybrid incompatibilities that enabled us to experimentally purify a genetically labeled A. gambiae Y chromosome in an A. arabiensis background. Whole genome sequencing (WGS) confirmed that the A. gambiae Y retained its original sequence content in the A. arabiensis genomic background. In contrast to comparable experiments in Drosophila, we find that the presence of a heterospecific Y chromosome has no significant effect on the expression of A. arabiensis genes, and transcriptional differences can be explained almost exclusively as a direct consequence of transcripts arising from sequence elements present on the A. gambiae Y chromosome itself. We find that Y hybrids show no obvious fertility defects, and no substantial reduction in male competitiveness. Our results demonstrate that, despite their radically different structure, Y chromosomes of these two species of the gambiae complex that diverged an estimated 1.85 MYA function interchangeably, thus indicating that the Y chromosome does not harbor loci contributing to hybrid incompatibility. Therefore, Y chromosome gene flow between members of the gambiae complex is possible even at their current level of divergence. Importantly, this also suggests that malaria control interventions based on sex-distorting Y drive would be transferable, whether intentionally or contingent, between the major malaria vector species.

KEYWORDS:

Y chromosome; gene flow; hybrid incompatibility; malaria; vector genetics

PMID:
28860320
PMCID:
PMC5629335
DOI:
10.1534/genetics.117.300221
[Indexed for MEDLINE]
Free PMC Article

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