Parallel evolution of behaviour during independent host-shifts following maize introduction into Asia and Europe.

Vincent Calcagno,Denis Bourguet,Philippe Audiot,Zhen-Ying Wang,Sergine Ponsard,Kang-Lai He,Gui-Zhen Gao,Zhao-Zhi Lu,Clémentine Mitoyen

doi:10.1111/eva.12481

Abstract

Maize was introduced into opposite sides of Eurasia 500 years ago, in Western Europe and in Asia. This caused two host‐shifts in the phytophagous genus Ostrinia; O. nubilalis (the European corn borer; ECB) and O. furnacalis (the Asian corn borer; ACB) are now major pests of maize worldwide. They originated independently from Dicot‐feeding ancestors, similar to O. scapulalis (the Adzuki bean borer; ABB). Unlike other host‐plants, maize is yearly harvested, and harvesting practices impose severe mortality on larvae found above the cut‐off line. Positive geotaxis in the ECB has been proposed as a behavioural adaptation to harvesting practices, allowing larvae to move below the cut‐off line and thus escape harvest mortality. Here, we test whether the same behavioural adaptation evolved independently in Europe and in Asia. We sampled eight genetically differentiated ECB, ACB and ABB populations in France and China and monitored geotaxis through the entire larval development in artificial stacks mimicking maize stems. We find that all ECB and ACB populations show a similar tendency to move down during the latest larval stages, a behaviour not observed in any European or Asian ABB population. The behaviour is robustly expressed regardless of larval density, development mode or environmental conditions. Our results indicate that maize introduction triggered parallel behavioural adaptations in Europe and Asia, harvest selection presumably being the main driver.

Highlights

Anthropogenic selection pressures can elicit fast adaptive responses, sometimes occurring over as few as a dozen generations (Palumbi, 2001)
Aphids Myzus persicae developed the capacity to discriminate fields treated with neonicotinoïds and adapt dispersal behaviour (Fray et al, 2014), and Diabrotica virgifera virgifera populations with reduced host fidelity have emerged following the implementation of corn-soya
Our results show that the two corn borer species, ACB in Asia and European corn borer (ECB) in Europe, have independently evolved a tendency to move down in the latest stages of their larval development

Summary

| INTRODUCTION

Anthropogenic selection pressures can elicit fast adaptive responses, sometimes occurring over as few as a dozen generations (Palumbi, 2001). Destroying maize stalks after harvesting was encouraged as a way to control the pest (Caffrey & Worthley, 1927) This situation has culminated in the last 100 years or so, following the wide adoption of mechanical harvesting: combined harvesters kill virtually all larvae above the cut-off line (Calcagno, Bonhomme, Thomas, Singer, & Bourguet, 2010; Chen, Song, Wang, & Wang, 2016). This dramatic vertical gradient in survival should exert a strong selection pressure for larvae to move closer to the ground prior to harvesting, which typically occurs at the end of larval development, just before the onset of diapause. We further tested whether the expression of the geotaxis phenotype depended on the developmental pathway taken by larvae (diapause vs. direct development)

| MATERIALS AND METHODS

Findings

| DISCUSSION