Hybridization and gene flow in the mega-pest lineage of moth, Helicoverpa

Abstract

Within the mega-pest lineage of heliothine moths are a number of polyphagous, highly mobile species for which the exchange of adaptive traits through hybridization would affect their properties as pests. The recent invasion of South America by one of the most significant agricultural pests, Helicoverpa armigera, raises concerns for the formation of novel combinations of adaptive genes following hybridization with the closely related Helicoverpa zea To investigate the propensity for hybridization within the genus Helicoverpa, we carried out whole-genome resequencing of samples from six species, focusing in particular upon H. armigera population structure and its relationship with H. zea We show that both H. armigera subspecies have greater genetic diversity and effective population sizes than do the other species. We find no signals for gene flow among the six species, other than between H. armigera and H. zea, with nine Brazilian individuals proving to be hybrids of those two species. Eight had largely H. armigera genomes with some introgressed DNA from H. zea scattered throughout. The ninth resembled an F1 hybrid but with stretches of homozygosity for each parental species that reflect previous hybridization. Regions homozygous for H. armigera-derived DNA in this individual included one containing a gustatory receptor and esterase genes previously associated with host range, while another encoded a cytochrome P450 that confers insecticide resistance. Our data point toward the emergence of novel hybrid ecotypes and highlight the importance of monitoring H. armigera genotypes as they spread through the Americas.

Keywords: gene flow; hybridization; pest; population genomics; selective sweep.

Fig. 1.

Maximum likelihood phylogenies for all six Helicoverpa species, calculated using 4D SNPs across autosomes. Interior nodes marked with a black circle represent bootstrap support greater than 50%.

Fig. 2.

Outgroup f₃ statistic for the model f₃ (H. armigera conferta; Brazilian hybrids, x), demonstrating shared genetic drift between Brazilian hybrids and individual H. armigera armigera (x). Error bars represent SEs.

Fig. 3.

Averages of 100 PSMC bootstrap estimates of effective population size for all species. The hybrids were not included in this analysis.

Fig. 4.

CLR plots screening for selective sweeps in (A) H. armigera armigera and (B) H. armigera conferta, where the significance thresholds are 36.6 and 34.9, respectively, as shown by dashed lines.

Fig. 5.

Profiles of f_D values calculated for 10-kb nonoverlapping windows across the genome for individuals A–L. Individual A is a European H. armigera. Individuals B and C are H. zea from the United States and Brazil, respectively. Individuals D–L are Brazilian hybrids, and their profiles provide evidence for hybridization between H. armigera and H. zea. Individual-specific metadata, including mitochondrial genotypes, are listed in Table S4.

Fig. 6.

HI across 250-kb windows for individual L, highlighting homozygosity indicating previous hybridization. SNPs segregating strongly between H. armigera armigera and H. zea were used to infer ancestry of individual L (black and gray), while calculations using all H. armigera armigera and H. zea (red and blue, respectively) are plotted for reference. Windows are considered significantly different from 0.5 where HI is above 0.598 or below 0.4375 (P < 5 × 10⁻⁷). The arrow highlights the lowest value of HI for individual L.