The redlegged earth mite draft genome provides new insights into pesticide resistance evolution and demography in its invasive Australian range

• Published in: Journal of evolutionary biology 2023-02, Vol.36 (2), p.381-398
• Main Authors: Thia, Joshua A., Korhonen, Pasi K., Young, Neil D., Gasser, Robin B., Umina, Paul A., Yang, Qiong, Edwards, Owain, Walsh, Tom, Hoffmann, Ary A.
• Format: Article
• Language: English
• Subjects: ACE protein; acetylcholinesterase; agricultural pests; Animals; Australia; Chemical pest control; Copy number; demographic inference; Demography; DNA Copy Number Variations; Evolution; gene amplification; Gene flow; Genetic diversity; Genetic markers; Genome; Genomes; Genomic analysis; Halotydeus destructor; invasive species; Mites; Mites - genetics; Mutation; Organophosphates; Pest control; Pesticide resistance; Pesticides; Pests; Population Dynamics; population genomics; Populations; Prediction models; Pyrethroids; Sodium channels
• ISSN: 1010-061X; 1420-9101
• DOI: 10.1111/jeb.14144

Genomic data provide valuable insights into pest management issues such as resistance evolution, historical patterns of pest invasions and ongoing population dynamics. We assembled the first reference genome for the redlegged earth mite, Halotydeus destructor (Tucker, 1925), to investigate adaptation to pesticide pressures and demography in its invasive Australian range using whole‐genome pool‐seq data from regionally distributed populations. Our reference genome comprises 132 autosomal contigs, with a total length of 48.90 Mb. We observed a large complex of ace genes, which has presumably evolved from a long history of organophosphate selection in H. destructor and may contribute towards organophosphate resistance through copy number variation, target‐site mutations and structural variants. In the putative ancestral H. destructor ace gene, we identified three target‐site mutations (G119S, A201S and F331Y) segregating in organophosphate‐resistant populations. Additionally, we identified two new para sodium channel gene mutations (L925I and F1020Y) that may contribute to pyrethroid resistance. Regional structuring observed in population genomic analyses indicates that gene flow in H. destructor does not homogenize populations across large geographic distances. However, our demographic analyses were equivocal on the magnitude of gene flow; the short invasion history of H. destructor makes it difficult to distinguish scenarios of complete isolation vs. ongoing migration. Nonetheless, we identified clear signatures of reduced genetic diversity and smaller inferred effective population sizes in eastern vs. western populations, which is consistent with the stepping‐stone invasion pathway of this pest in Australia. These new insights will inform development of diagnostic genetic markers of resistance, further investigation into the multifaceted organophosphate resistance mechanism and predictive modelling of resistance evolution and spread.