Genomewide transcriptional signatures of migratory flight activity in a globally invasive insect pest.

Christopher M Jones,Ka S Lim,Chris Bass,John G Oakeshott,John Vontas,Jason W Chapman,Yihua Yang,Alexie Papanicolaou,George K Mironidis

doi:10.1111/mec.13362

Abstract

Migration is a key life history strategy for many animals and requires a suite of behavioural, morphological and physiological adaptations which together form the ‘migratory syndrome’. Genetic variation has been demonstrated for many traits that make up this syndrome, but the underlying genes involved remain elusive. Recent studies investigating migration‐associated genes have focussed on sampling migratory and nonmigratory populations from different geographic locations but have seldom explored phenotypic variation in a migratory trait. Here, we use a novel combination of tethered flight and next‐generation sequencing to determine transcriptomic differences associated with flight activity in a globally invasive moth pest, the cotton bollworm Helicoverpa armigera. By developing a state‐of‐the‐art phenotyping platform, we show that field‐collected H. armigera display continuous variation in flight performance with individuals capable of flying up to 40 km during a single night. Comparative transcriptomics of flight phenotypes drove a gene expression analysis to reveal a suite of expressed candidate genes which are clearly related to physiological adaptations required for long‐distance flight. These include genes important to the mobilization of lipids as flight fuel, the development of flight muscle structure and the regulation of hormones that influence migratory physiology. We conclude that the ability to express this complex set of pathways underlines the remarkable flexibility of facultative insect migrants to respond to deteriorating conditions in the form of migratory flight and, more broadly, the results provide novel insights into the fundamental transcriptional changes required for migration in insects and other taxa.

Highlights

The ability to initiate and sustain periods of long-distance flight is a prerequisite for the billions of insects that migrate each year (Chapman et al 2012, 2015)
To dissect the molecular basis of flight in a migratory insect, we focus here on the propensity for long-distance flight and use an unique integrative approach of tethered flight and transcriptomics to (i) quantify the intraspecific variation in flight activity during the migratory phase of recently collected field populations of H. armigera from different geographic origins, (ii) identify the differentially expressed suite of genes between flight phenotypes that contribute to the migratory capacity of H. armigera and (iii) validate the expression of these genes in independently flown H. armigera adults
The adult H. armigera used in the flight mill, RNA-seq and qPCR experiments were collected from Bt cotton from five populations in China [Dafeng (Jiangsu province), Anyang (Henan province), Jingzhou, (Hubei province), Qiuxian (Hebei province) and Wanjiang (Anhui province)] and a single site in northern Greece during the summer of 2013 and shipped to Rothamsted Research, UK (Table S1, Supporting information)

Summary

Introduction

The ability to initiate and sustain periods of long-distance flight is a prerequisite for the billions of insects that migrate each year (Chapman et al 2012, 2015). The behavioural, physiological and morphological adaptations necessary to undertake such flights form part of a much larger inherited ‘migratory syndrome’ which is present across the Insecta and in other animal migrants such as birds and fish (Roff & Fairbairn 2007; Dingle 2014). Range of taxa have shown that there is significant phenotypic and genetic variation in the individual traits that comprise the migratory syndrome (Pulido et al 1996; Roff & Fairbairn 2007). The genes and associated biochemical pathways that underpin this variation, remain poorly understood

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Results