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Genomic innovations, transcriptional plasticity and gene loss underlying the evolution and divergence of two highly polyphagous and invasive Helicoverpa pest species

S. L. Pearce 1 D. F. Clarke 1, 2 P. D. East 1 S. Elfekih 1 K. H. J. Gordon 1 L. S. Jermiin 1 A. Mcgaughran 1, 3 J. G. Oakeshott 1 A. Papanikolaou 1 O. P. Perera 4 R. V. Rane 1, 2 S. Richards 5 W. T. Tay 1 T. K. Walsh 1 A. Anderson 1 C. J. Anderson 1, 6 S. Asgari 7 P. G. Board 8 A. Bretschneider 9 P. M. Campbell 1 Thomas Chertemps 10 J. T. Christeller 11 C. W. Coppin 1 S. J. Downes 1 G. Duan 12 C. A. Farnsworth 1 R. T. Good 13 L. B. Han 14 Y. C. Han 1, 15 K. Hatje 16 I. Horne 1 Y. P. Huang 17 D. S. T. Hughes 18 Emmanuelle Joly 10 W. James 1 S. Jhangiani 18 M. Kollmar 16 S. S. Kuwar 9 S. Li 1 N-Y. Liu 1, 19 Martine Maibeche Coisne 10 J. R. Miller 20 N. Montagne 21 T. Perry 13 J. Qu 18 S. V. Song 13 G. G. Sutton 20 H. Vogel 9 B. P. Walenz 20 W. Xu 1, 22 H-J. Zhang 1, 23 Z. Zou 14 P. Batterham 13 O. R. Edwards 1 R. Feyereisen 24 R. A. Gibbs 18 D. G. Heckel 9 A. Mcgrath 1 C. Robin 13 S. E. Scherer 18 K. C. Worley 18 Y. D. Wu 15
Abstract : Background: Helicoverpa armigera and Helicoverpa zea are major caterpillar pests of Old and New World agriculture, respectively. Both, particularly H. armigera, are extremely polyphagous, and H. armigera has developed resistance to many insecticides. Here we use comparative genomics, transcriptomics and resequencing to elucidate the genetic basis for their properties as pests. Results: We find that, prior to their divergence about 1.5 Mya, the H. armigera/H. zea lineage had accumulated up to more than 100 more members of specific detoxification and digestion gene families and more than 100 extra gustatory receptor genes, compared to other lepidopterans with narrower host ranges. The two genomes remain very similar in gene content and order, but H. armigera is more polymorphic overall, and H. zea has lost several detoxification genes, as well as about 50 gustatory receptor genes. It also lacks certain genes and alleles conferring insecticide resistance found in H. armigera. Non-synonymous sites in the expanded gene families above are rapidly diverging, both between paralogues and between orthologues in the two species. Whole genome transcriptomic analyses of H. armigera larvae show widely divergent responses to different host plants, including responses among many of the duplicated detoxification and digestion genes. Conclusions: The extreme polyphagy of the two heliothines is associated with extensive amplification and neofunctionalisation of genes involved in host finding and use, coupled with versatile transcriptional responses on different hosts. H. armigera's invasion of the Americas in recent years means that hybridisation could generate populations that are both locally adapted and insecticide resistant.
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S. L. Pearce, D. F. Clarke, P. D. East, S. Elfekih, K. H. J. Gordon, et al.. Genomic innovations, transcriptional plasticity and gene loss underlying the evolution and divergence of two highly polyphagous and invasive Helicoverpa pest species. BMC Biology, BioMed Central, 2017, 15, ⟨10.1186/s12915-017-0402-6⟩. ⟨hal-02629185⟩

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