Genomic signatures underlying successful host shift of a parasite

Authors: ZHENG, HUOQING - Zhejiang University; WANG, SHUAI - Zhejiang University; WU, YUQI - Zhejiang University; ZOU, SHENGMEI - Zhejiang University; DIETEMANN, VINCENT - Agroscope; NEUMANN, PETER - Agroscope; Chen, Yanping - Judy; Evans, Jay; HU, FULIANG - Zhejiang University; FENG, YE - Zhejiang University

Submitted to: Nature Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/22/2022
Publication Date: 5/4/2022
Citation: Zheng, Huoqing, Wang, Shuai, Wu, Yuqi, Zou, Shengmei, Dietemann, Vincent, Neumann, Peter, Chen, Y., Evans, J.D., Hu, Fuliang, Feng, Ye 2022. Genomic signatures underlying successful host shift of a parasite. Nature Communications. 1-11. https://doi.org/10.1016/j.jare.2022.04.014.
DOI: https://doi.org/10.1016/j.jare.2022.04.014

Interpretive Summary: Host shift of pathogens can have devastating consequences for infected organisms. The parasitic mite Varroa destructor shifted from its original host, Eastern honey bees, to Western honey bees, rapidly colonizing in these bees and becoming the key cause of colony mortality worldwide. However, the mechanisms underlying successful host shift and reproduction of the Varroa mite within Western honey bees have not been fully studied. As part of this study, we conducted a genetic study of Varroa mites collected from five different countries across four continents. The novel insights of this study will improve our understanding of the origin and evolution of the Varroa mite. Furthermore, the genetic information gained from this study will contribute to the rational design of novel methods to keep Varroa populations under control and should be of interest to the researchers, graduate students, beekeepers and policymakers worldwide.

Technical Abstract: Host shifts of parasites can cause devastating effects on novel hosts, but in many cases the underlying mechanisms enabling successful shifts remain poorly understood. Ectoparasitic mites, Varroa destructor, shifted hosts from Eastern honey bees (Apis cerana) to Western honey bees (Apis mellifera). In the novel hosts, mite reproduction is enhanced, thereby leading to colony death and causing a major threat to global apiculture. However, despite common drifting of mites between host species, the mechanisms governing enhanced mite reproduction (i.e. virulence) and underlying the rare successful host shifts are unknown. Here, we combined infestation experiments with genomics and transcriptomics of two closely related mite lineages, one having shifted hosts, the other not, to investigate the genomic basis of differential ovary activation, which underlies the impact on host colonies. We show that mutations at five candidate loci tightly associate to ovary activation of V. destructor in its new host and could be linked to the successful host shift. The data revealed that up-regulation of oogenesis in brood cells of the novel hosts is related to the genes Vitellogenin 6-like and Bent and to core regulatory networks including the proteins CG5800, DAP160 and SAS10. Genetically determined differences in parasite ovary activation appear to be the key mechanism explaining this successful host shift.