When History Repeats Itself: Exploring the Genetic Architecture of Host-Plant Adaptation in Two Closely Related Lepidopteran Species

Hermine Alexandre,Réjane Streiff,Sandrine Cros-Arteil,Sergine Ponsard,Denis Bourguet,Renaud Vitalis,Philippe Audiot,Casper Breuker

doi:10.1371/journal.pone.0069211

Abstract

The genus Ostrinia includes two allopatric maize pests across Eurasia, namely the European corn borer (ECB, O. nubilalis) and the Asian corn borer (ACB, O. furnacalis). A third species, the Adzuki bean borer (ABB, O. scapulalis), occurs in sympatry with both the ECB and the ACB. The ABB mostly feeds on native dicots, which probably correspond to the ancestral host plant type for the genus Ostrinia. This situation offers the opportunity to characterize the two presumably independent adaptations or preadaptations to maize that occurred in the ECB and ACB. In the present study, we aimed at deciphering the genetic architecture of these two adaptations to maize, a monocot host plant recently introduced into Eurasia. To this end, we performed a genome scan analysis based on 684 AFLP markers in 12 populations of ECB, ACB and ABB. We detected 2 outlier AFLP loci when comparing French populations of the ECB and ABB, and 9 outliers when comparing Chinese populations of the ACB and ABB. These outliers were different in both countries, and we found no evidence of linkage disequilibrium between any two of them. These results suggest that adaptation or preadaptation to maize relies on a different genetic architecture in the ECB and ACB. However, this conclusion must be considered in light of the constraints inherent to genome scan approaches and of the intricate evolution of adaptation and reproductive isolation in the Ostrinia spp. complex.

Highlights

An intriguing yet unresolved question in evolutionary biology is the degree to which evolution is canalized by intrinsic developmental properties [1]
Most loci were shared between host-plants within countries, with only 6%, 7%, 5% and 1.5% of the loci being private to French samples on maize, French samples on dicots, Chinese samples on maize and Chinese samples on dicots, respectively
Overall, our results suggest that adaptation to maize has a different genetic architecture in the Asian corn borer (ACB) and European corn borer (ECB)

Summary

Introduction

An intriguing yet unresolved question in evolutionary biology is the degree to which evolution is canalized by intrinsic developmental properties [1]. Somewhat difficult, an alternative approach is to study naturally occurring cases of repeated adaptations, i.e. adaptations that occurred independently as a response to similar ecological changes. Evolutionary biologists considered that a trait evolving in closely related lineages (‘parallel evolution’) is likely to rely on the same genetic architecture, whereas a trait evolving in already distant lineages (‘convergent evolution’) is more likely to involve different genetic architectures. Some case studies showed that the same gene can be involved in similar adaptations in phylogenetically distant taxa (e.g., the MC1R gene involved in color variation in lizards, birds, felids, mice and black bears [5]). With the advent of next-generation sequencing technologies, it is possible to get insight into the genetic architecture of repeated adaptations, regardless of their occurrence in closely or more distantly related taxa

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