Molecular phylogenetics of heliothine moths (Lepidoptera: Noctuidae: Heliothinae), with comments on the evolution of host range and pest status

Abstract

Abstract. The Heliothinae are a cosmopolitan subfamily of about 365 species that include some of the world's most injurious crop pests. This study re-assesses evolutionary relationships within heliothines, providing an improved phylogeny and classification to support ongoing intensive research on heliothine genomics, systematics, and biology. Our phylogeny estimate is based on two nuclear gene regions, namely elongation factor-1a (EF-1a; 1240 bp) and dopa decarboxylase (DDC; 687 bp), and on the barcoding region of mitochondrial cytochrome oxidase I (COI; 708 bp), providing a total of 2635 bp. These were sequenced for 71 heliothines, representing all major genera and nearly all recognized subgenera and species groups, and for 16 outgroups representing all major lineages of trifine Noctuidae. Analysis of the combined data by maximum likelihood, unweighted parsimony and Bayesian methods gave nearly identical topologies, and the individual gene trees showed only one case of potentially strong conflict. Relationships among genera and subgenera are resolved with strong bootstrap support. The earliest-diverging lineages (c. 200 species in total) consist almost entirely of host specialists, reflecting the inferred ancestral heliothine host range under parsimony. The remaining species form a clade -the Heliothis group -that includes most of the polyphages (30% of heliothines) and all of the major pests. Many other species in the Heliothis group, however, are host specialists. Our results extend previous efforts to subdivide this large clade, and show the most notorious pest groups, the corn earworm complex (Helicoverpa) and the tobacco budworm (Heliothis virescens) group, to be closely related, joining with a small oligophagous genus in what we term the major-pest lineage. Thus, genomic/ experimental results from one model pest may extrapolate well to other pest species. The frequency of evolutionary expansion and contraction in host range appears to increase dramatically at the base of the Heliothis group, in contrast to the case for earlier-diverging lineages. We ascribe this difference provisionally to differential evolutionary constraints arising from contrasting life-history syndromes. Host-specific behaviour and crypsis, coupled with low fecundity and vagility, may discourage host-range expansion in earlier-diverging lineages. By Systematic EntemologySystematic Entomology contrast, in the Heliothis group, the absence of host-specific traits, coupled with high vagility and fecundity, may more readily permit expansion or contraction of the host range in response to varying ecological pressures such as host species abundance or differential competition and predation.

High nucleotide diversity and limited linkage disequilibrium in Helicoverpa armigera facilitates the detection of a selective sweep

“…However, population structures and levels of diversity in H. punctigera and H. assulta are not as well characterized -the provenance of the H. armigera divergent allele could be a cryptic race or isolated population of either species given their overlapping ranges. Alternatively, it could be from another species not characterized here such as Helicoverpa hardwicki, Helicoverpa prepodes and members of the genus Australothis and Heliocheilus, which are endemic to Australia (Matthews, 1999;Cho et al, 2008).…”

“…Helicoverpa is a well-defined genus within the heliothine subfamily of noctuid moths where its monophyly is strongly supported by morphology and molecular characterization (Matthews, 1999;Cho et al, 2008). Within the genus, however, relationships between species are less clear often due to morphological similarities.…”

Genetic diversity and susceptibility to Vip3Aa20 protein in Brazilian populations of <i>Helicoverpa armigera</i> and <i>Helicoverpa zea</i> (Lepidoptera: Noctuidae)

“…These results suggest the rapid evolution of some primer biding sites in both species' genomes. This genetic divergence between the species is a paradox because they are able to produce fertile hybrid offspring in the laboratory (LASTER; HARDEE, 1995;SHENG, 1995;CHO et al, 2008;POGUE, 2013).…”

“…armigera and H. zea are considered sibling species as they are phylogenetically close POOLE;MATTHEWS, 1993;CHO et al, 2008).…”

“…The Heliothinae (Lepidoptera: Noctuidae) subfamily has 381 described species, many of which are important agricultural pests from the Helicoverpa MATTHEWS, 1993;HARDEE, 1995;SHENG, 1995;CHO, S. et al, 2008). Some hypotheses propose that H. zea evolved from a small portion of the larger H. armigera population (i.e., a "founder effect") that reached the American continent approximately 1.5 million years ago, which is consistent with previous phylogeographic analyses of H. armigera and H. zea individuals (MALLET et al, 1993;.…”