‘Becoming a species by becoming a pest’ or how two maize pests of the genus Ostrinia possibly evolved through parallel ecological speciation events

Abstract

New agricultural pest species attacking introduced crops may evolve from pre-existing local herbivores by ecological speciation, thereby becoming a species by becoming a pest. We compare the evolutionary pathways by which two maize pests (the Asian and the European corn borers, ACB and ECB) in the genus Ostrinia (Lepidoptera, Crambidae) probably diverged from an ancestral species close to the current Adzuki bean borer (ABB). We typed larval Ostrinia populations collected on maize and dicotyledons across China and eastern Siberia, at microsatellite and mitochondrial loci. We found only two clusters: one on maize (as expected) and a single one on dicotyledons despite differences in male mid-tibia morphology, suggesting that all individuals from dicotyledons belonged to the ABB. We found evidence for migrants and hybrids on both host plant types. Hybrids suggest that field reproductive isolation is incomplete between ACB and ABB. Interestingly, a few individuals with an 'ABB-like' microsatellite profile collected on dicotyledons had 'ACB' mtDNA rather than 'ABB-like' mtDNA, whereas the reverse was never found on maize. This suggests asymmetrical gene flow directed from the ACB towards the ABB. Hybrids and backcrosses in all directions were obtained in no-choice tests. In laboratory conditions, they survived as well as parental strain individuals. In Xinjiang, we found ACB and ECB in sympatry, but no hybrids. Altogether, our results suggest that reproductive isolation between ACB and ABB is incomplete and mostly prezygotic. This points to ecological speciation as a possible evolutionary scenario, as previously found for ECB and ABB in Europe.

Influence of host plant, geography and pheromone strain on genomic differentiation in sympatric populations of Ostrinia nubilalis

“…Ostrinia nubilalis is an emerging model for speciation dynamics due to sympatric ecotypes or strains that vary in voltinism and sex‐pheromone communication (Coates et al, ; Dopman et al, ; Kozak et al, ; Lassance, ; Olsson et al, ). Ecological differences in host plant preference occur between closely related O. nubilalis strains in North America (O'Rourke et al, ) and among Ostrinia species in Europe (Bethenod et al, ; Bourguet, Bethenod, Trouve, & Viard, ; Bourguet et al, ; Frolov et al, ; Pélozuelo, Malosse, Genestier, Guenego, & Frérot, ; Pélozuelo et al, ; Thomas, Bethenod, Pelozuelo, Frérot, & Bourguet, ). Although pheromone system and host plant use co‐vary in Ostrinia (Alexandre et al, ), elucidating the relative contribution of various selective forces to differentiation in the presence of high rates of gene flow remains a challenge.…”

“…In France, Ostrinia populations using the alternative pheromone blends of E11‐ and Z11‐14:OAc were initially assumed to be E‐ and Z‐strain O. nubilalis . Strong associations were demonstrated among moths using the Z‐pheromone communication system for maize (C4) and the E‐system moths for C3 host plants (Bontemps et al, ; Bourguet et al, ) which were accompanied by significant levels of genetic differentiation (Bethenod et al, ; Malausa et al, ). However, subsequent studies concluded that Ostrinia using the E‐pheromone system in France were O. scapulalis , and a different species compared to sympatric Z‐strain O. nubilalis (Calcagno, Bonhomme, Thomas, Singer, & Bourguet, ; Frolov, Bourguet, & Ponsard, ; Malausa et al, ).…”

Crop domestication, global human-mediated migration, and the unresolved role of geography in pest control

“…Moth populations on maize are reproductively isolated from populations that feed on mugwort (Calcagno et al, 2007;Bourguet et al, 2014). The two host races also appear to be genetically isolated.…”

“…Native herbivore populations that shift onto agricultural crops can become genetically differentiated from populations that remain on the original host plant (Vialatte et al, 2005;Michel et al, 2010;Lavandero et al, 2011 Midamegbe et al, 2011;Barman et al, 2012;Bourguet et al, 2014). Because host shifts create new ecological opportunities for herbivores, population can diverge via ecological speciation in sympatry (Bush, 1969;Berlocher and Feder, 2002).…”

“…B) Insects may host shift from their original host plant onto an introduced crop plant. Example: the European corn borer, Ostrinia nubilalis (Lepidoptera: Crambidae) shifted from feeding on mugwort (Artemisia vulgaris L.) and hop (Humulus lupulus L.) onto maize following its introduction into Europe in the 1500s (Bourguet et al, 2014). C) Insect herbivores associated with the crop plant can be introduced to other cropping regions around the world.…”