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

Authors: PEARCE, S.L. - COMMONWEALTH SCIENTIFIC AND INDUSTRIAL RESEARCH ORGANISATION (CSIRO); CLARK, D.F. - COMMONWEALTH SCIENTIFIC AND INDUSTRIAL RESEARCH ORGANISATION (CSIRO); EAST, P.D. - COMMONWEALTH SCIENTIFIC AND INDUSTRIAL RESEARCH ORGANISATION (CSIRO); ELFEKIH, S. - COMMONWEALTH SCIENTIFIC AND INDUSTRIAL RESEARCH ORGANISATION (CSIRO); GORDON, K.H.J. - COMMONWEALTH SCIENTIFIC AND INDUSTRIAL RESEARCH ORGANISATION (CSIRO); JERMIIN, L.S. - COMMONWEALTH SCIENTIFIC AND INDUSTRIAL RESEARCH ORGANISATION (CSIRO); MCGAUGHRAN, A. - COMMONWEALTH SCIENTIFIC AND INDUSTRIAL RESEARCH ORGANISATION (CSIRO); OAKESHOTT, J.G. - COMMONWEALTH SCIENTIFIC AND INDUSTRIAL RESEARCH ORGANISATION (CSIRO); PAPANIKOLAOU, A. - COMMONWEALTH SCIENTIFIC AND INDUSTRIAL RESEARCH ORGANISATION (CSIRO); Perera, Omaththage

Submitted to: BMC Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/4/2017
Publication Date: 7/31/2017
Publication URL: https://handle.nal.usda.gov/10113/5801799
Citation: Pearce, S., Clark, D., East, P., Elfekih, S., Gordon, K., Jermiin, L., Mcgaughran, A., Oakeshott, J., Papanikolaou, A., Perera, O.P. 2017. Genomic basis for the pest status of two Helicoverpa species. BMC Biology. 15:63. https://doi.org/10.1186/s12915-017-0402-6.
DOI: https://doi.org/10.1186/s12915-017-0402-6

Interpretive Summary: Old world bollworm, Helicoverpa armigera, and the bollworm, Helicoverpa zea, cause significant damage to a number of crops due to their ability to feed on a wide range of host plants. Control of these pests is often difficult due to their high tolerance to chemical and biological insecticides. Genomes of both bollworm were sequenced and assembled and gene organization was studied. It was found that H. zea has lost several detoxification genes and more than 50 gustatory receptor genes after the two species diverged from a common ancestor about 1.5 million years ago. Additional detoxification genes present in H. armigera has helped that species to feed on a broader host range than H. zea and develop resistance to several insecticides. Hybridization of H. zea with H. armigera in geographies where H. armigera has invaded recently could lead to transfer of some of the detoxification genes to H. zea, making it more resistant to insecticides.

Technical 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 and population genomics and transcriptomics to elucidate the genetic basis for their properties as pests. Results: We found that, prior to their divergence about 1.5 Mya, the H. armigera/H. zea lineage had accumulated up to over 100 more genes in specific detoxification and digestion families, and over 100 extra gustatory receptor genes, than 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 above expanded gene families 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 among many of the duplicated detoxification and digestion genes. Conclusions: The extreme polyphagy of the two heliothines is associated with extensive amplification and neo-functionalisation 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 introgression of specific genes, such as for gustatory receptors and resistance, could broaden the ecological niche and exacerbate the pest status of H. zea.