Revisiting the evolution of Ostrinia moths with phylogenomics (Pyraloidea: Crambidae: Pyraustinae)

Abstract

Reconstructing a robust phylogenetic framework is key to understanding the ecology and evolution of many economically important taxa. The crambid moth genus Ostrinia contains multiple agricultural pests, and its classification and phylogeny has remained controversial because of the paucity of characters and the lack of clear morphological boundaries for its species. To address these issues, we inferred a molecular phylogeny of Ostrinia using a phylogenomic dataset containing 498 loci and 115 197 nucleotide sites and examined whether traditional morphological characters corroborate our molecular results. Our results strongly support the monophyly of one of the Ostrinia species groups but surprisingly do not support the monophyly of the other two. Based on the extensive morphological examination and broadly representative taxon sampling of the phylogenomic analyses, we propose a revised classification of the genus, defined by three species groups (Ostrinia nubilalis species group, Ostrinia obumbratalis species group, and Ostrinia penitalis species group), which differs from the traditional classification of Mutuura & Munroe (1970). Morphological and molecular evidence reveal the presence of a new North American species, Ostrinia multispinosa Yang sp.n., closely related to O. obumbratalis. Our analyses indicate that the Ostrinia ancestral larval host preference was for dicots, and that O. nubilalis (European corn borer) and Ostrinia furnacalis (Asian corn borer) independently evolved a preference for feeding on monocots (i.e., maize). Males of a few Ostrinia species have enlarged, grooved midtibiae with brush organs that are known to attract females to increase mating success during courtship, which may represent a derived condition. Our study provides a strong evolutionary framework for this agriculturally important insect lineage.

Two complete genomes of male-killing Wolbachia infecting Ostrinia moth species illuminate their evolutionary dynamics and association with hosts

“…Historically, the genus was largely classified into three groups and are denoted by the letters I, II, and III, according to the morphology of male genitalia (Mutuura & Munroe 1970). However, a recent phylogenomic study confirmed the monophyly of only group III and proposed a new classification system in which the genus is divided into three new species groups (Clade I, II, and III) (Yang et al 2021). All species of group III (Mutuura & Munroe, 1970) were incorporated into Clade III, the Ostrinia nubilalis species group, along with some previously classified species in group II.…”

“…Both O. furnacalis (Asian corn borer) and O. scapulalis (Adzuki bean borer), classified as group III or the new Clade III, are important agricultural pests. O. furnacalis is a significant maize pest in Asia, causing substantial economic damage, whereas O. scapulalis attacks some crops such as hops, hemp and legumes (Ishikawa et al 1999; Yang et al 2021).…”

Multilocus evidence provides insight into the demographic history and asymmetrical gene flow between Ostrinia furnacalis and Ostrinia nubilalis (Lepidoptera: Crambidae) in the Yili area, Xinjiang, China

“…The ACB (Asian corn borer), O. furnacalis (Guenée), and the ECB (European corn borer), O. nubilalis (Hübner) (Crambidae: Pyraustinae), are worldwide maize pests that cause substantial yield losses in corn production (Bourguet et al, 2014 ; Frolov et al, 2007 ; Mutuura & Munroe, 1970 ). These two corn borers both belong to the O. nubilalis species group (trilobed uncus of male genitalia, which is a structure derived from the 10th abdominal tergite to grasp the female during copulation; see Yang et al, 2021 : 830, Clade III in Figure 1 ), one of the most evolutionarily and ecologically interesting but taxonomically difficult groups in Lepidoptera. The species group includes 10 species and 23 subspecies worldwide (Frolov et al, 2007 ; Mutuura & Munroe, 1970 ; Yang et al, 2021 ).…”

“…These two corn borers both belong to the O. nubilalis species group (trilobed uncus of male genitalia, which is a structure derived from the 10th abdominal tergite to grasp the female during copulation; see Yang et al, 2021 : 830, Clade III in Figure 1 ), one of the most evolutionarily and ecologically interesting but taxonomically difficult groups in Lepidoptera. The species group includes 10 species and 23 subspecies worldwide (Frolov et al, 2007 ; Mutuura & Munroe, 1970 ; Yang et al, 2021 ). Incongruence between molecular phylogenetic relationships and the traditional classification of Ostrinia has been puzzling for a long time, leading to a number of members including ACB and ECB being morphologically indistinguishable and making accurate species identification extremely difficult (Hoshizaki et al, 2008 ; Kim et al, 1999 ; Mutuura & Munroe, 1970 ; Wang et al, 2017 ; Yang et al, 2021 ).…”

“…The species group includes 10 species and 23 subspecies worldwide (Frolov et al, 2007 ; Mutuura & Munroe, 1970 ; Yang et al, 2021 ). Incongruence between molecular phylogenetic relationships and the traditional classification of Ostrinia has been puzzling for a long time, leading to a number of members including ACB and ECB being morphologically indistinguishable and making accurate species identification extremely difficult (Hoshizaki et al, 2008 ; Kim et al, 1999 ; Mutuura & Munroe, 1970 ; Wang et al, 2017 ; Yang et al, 2021 ). On the other hand, this species complex is a good example to understand biogeographic patterns and evolutionary histories owing to their distributional complexity of the world.…”