Genomic evidence of sex chromosome aneuploidy and infection-associated genotypes in the tsetse fly Glossina fuscipes, the major vector of African trypanosomiasis in Uganda

• Authors: Norah P. Saarman, Utah State University; Jae Hak Son, The State University of New Jersey; Hongyu Zhao, Yale University; Luciano V. Cosme, Yale University; Yong Kong, Yale University; Mo Li, Yale University; Shiyu Wang, Emory University; Brian L. Weiss, Yale University; Richard Echodu, Gulu University; Robert Opiro, Gulu University; Serap Aksoy, Yale University; Adalgisa Caccone, Yale University
• Journal Title: Infection, Genetics and Evolution
• Volume: Volume 114
• Publisher: Elsevier | 2023-09-12, Pages 105501-None
• Type of Work: Article | Post-print: After Peer Review
• Publisher DOI: http://doi.org/10.1016/j.meegid.2023.105501
• Subjects: Biology, Genetics
• Keywords: ddRAD; Trypanosomiasis; Vector; Genome wide association; GWAS; Population genomics; Muller elements; Chromosome arms; Aneuploidy

Abstract

The primary vector of the trypanosome parasite causing human and animal African trypanosomiasis in Uganda is the riverine tsetse fly Glossina fuscipes fuscipes (Gff). Our study improved the Gff genome assembly with whole genome 10× Chromium sequencing of a lab reared pupae, identified autosomal versus sex-chromosomal regions of the genome with ddRAD-seq data from 627 field caught Gff, and identified SNPs associated with trypanosome infection with genome-wide association (GWA) analysis in a subset of 351 flies. Results from 10× Chromium sequencing greatly improved Gff genome assembly metrics and assigned a full third of the genome to the sex chromosome. Results from ddRAD-seq suggested possible sex-chromosome aneuploidy in Gff and identified a single autosomal SNP to be highly associated with trypanosome infection. The top associated SNP was ~1100 bp upstream of the gene lecithin cholesterol acyltransferase (LCAT), an important component of the molecular pathway that initiates trypanosome lysis and protection in mammals. Results suggest that there may be naturally occurring genetic variation in Gff in genomic regions in linkage disequilibrium with LCAT that can protect against trypanosome infection, thereby paving the way for targeted research into novel vector control strategies that can promote parasite resistance in natural populations.