Genomic signatures underlying the oogenesis of the ectoparasitic mite Varroa destructor on its new host Apis mellifera

Huoqing Zheng; Shuai Wang; Yuqi Wu; Shengmei Zou; Vincent Dietemann; Peter Neumann; Yanping Chen; Hongmei Li-Byarlay; Christian Pirk; Jay Evans; Fuliang Hu; Ye Feng

doi:10.1016/j.jare.2022.04.014

Genomic signatures underlying the oogenesis of the ectoparasitic mite Varroa destructor on its new host Apis mellifera

J Adv Res. 2023 Feb:44:1-11. doi: 10.1016/j.jare.2022.04.014. Epub 2022 May 4.

Authors

Huoqing Zheng¹, Shuai Wang¹, Yuqi Wu¹, Shengmei Zou², Vincent Dietemann³, Peter Neumann⁴, Yanping Chen⁵, Hongmei Li-Byarlay⁶, Christian Pirk⁷, Jay Evans⁵, Fuliang Hu¹, Ye Feng²

Affiliations

¹ College of Animal Sciences, Zhejiang University, Hangzhou, China.
² Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China; Institute for Translational Medicine, Zhejiang University School of Medicine, Hangzhou, China.
³ Swiss Bee Research Center, Agroscope, Bern, Switzerland; Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland.
⁴ Swiss Bee Research Center, Agroscope, Bern, Switzerland; Institute of Bee Health, Vetsuisse Faculty, University of Bern, Bern, Switzerland.
⁵ USDA-ARS Bee Research Laboratory, Beltsville, MD, USA.
⁶ Agricultural Research and Development Program, Central State University, Wilberforce, OH 45384, USA; Department of Agricultural and Life Science, Central State University, Wilberforce, OH 45384, USA.
⁷ Department of Zoology and Entomology, University of Pretoria, Pretoria, South Africa.

Abstract

Introduction: Host shift of parasites may have devastating effects on the novel hosts. One remarkable example is that of the ectoparasitic mite Varroa destructor, which has shifted its host from Eastern honey bees (Apis cerana) to Western honey bees (Apis mellifera) and posed a global threat to apiculture.

Objectives: To identify the genetic factors underlying the reproduction of host-shifted V. destructor on the new host.

Methods: Genome sequencing was conducted to construct the phylogeny of the host-shifted and non-shifted mites and to screen for genomic signatures that differentiated them. Artificial infestation experiment was conducted to compare the reproductive difference between the mites, and transcriptome sequencing was conducted to find differentially expressed genes (DEGs) during the reproduction process.

Results: The host-shifted and non-shifted V. destructor mites constituted two genetically distinct lineages, with 15,362 high-F_ST SNPs identified between them. Oogenesis was upregulated in host-shifted mites on the new host A. mellifera relative to non-shifted mites. The transcriptomes of the host-shifted and non-shifted mites differed significantly as early as 1h post-infestation. The DEGs were associated with nine genes carrying nonsynonymous high-F_ST SNPs, including mGluR2-like, Lamb2-like and Vitellogenin 6-like, which were also differentially expressed, and eIF4G, CG5800, Dap160 and Sas10, which were located in the center of the networks regulating the DEGs based on protein-protein interaction analysis.

Conclusions: The annotated functions of these genes were all associated with oogenesis. These genes appear to be the key genetic determinants of the oogenesis of host-shifted mites on the new host. Further study of these candidate genes will help elucidate the key mechanism underlying the success of host shifts of V. destructor.

Keywords: Honey bee; Host shift; Oogenesis; Transcriptome; Varroa destructor.

Publication types

Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Animals
Bees* / parasitology
Genome
Genomics
Oogenesis / genetics
Parasites* / genetics
Varroidae* / genetics