Genome-wide transcriptomic changes reveal the genetic pathways involved in insect migration

Abstract

Insects are capable of extraordinary feats of long-distance movement that have profound impacts on the function of terrestrial ecosystems. The ability to undertake these movements arose multiple times through the evolution of a suite of traits that make up the migratory syndrome, however the underlying genetic pathways involved remain poorly understood. Migratory hoverflies (Diptera: Syrphidae) are an emerging model group for studies of migration. They undertake seasonal movements in huge numbers across large parts of the globe and are important pollinators, biological control agents and decomposers. Here, we assembled a high-quality draft genome of the marmalade hoverfly (Episyrphus balteatus). We leveraged this genomic resource to undertake a genome-wide transcriptomic comparison of actively migrating Episyrphus, captured from a high mountain pass as they flew south to overwinter, with the transcriptomes of summer forms which were non-migratory. We identified 1543 genes with very strong evidence for differential expression. Interrogation of this gene set reveals a remarkable range of roles in metabolism, muscle structure and function, hormonal regulation, immunity, stress resistance, flight and feeding behaviour, longevity, reproductive diapause and sensory perception. These features of the migrant phenotype have arisen by the integration and modification of pathways such as insulin signalling for diapause and longevity, JAK/SAT for immunity, and those leading to octopamine production and fuelling to boost flight capabilities. Our results provide a powerful genomic resource for future research, and paint a comprehensive picture of global expression changes in an actively migrating insect, identifying key genomic components involved in this important life-history strategy.

Keywords: differential gene expression; genetics of migration; insect migration; migratory hoverflies; molecular adaptations; syrphidae.

FIGURE 1

Marmalade hoverfly migration. (a) A female marmalade hovefly, Episyrphus balteatus, feeding on a buttercup. (b) Location of the mountain pass of Bujaruelo (Puerto de Bujaruelo; red arrow), a 2273 m pass on the French–Spanish border in the Pyrenees (red box). Image from Google Maps. (c) The 30 m wide pass of Bujaruelo concentrates migrants crossing the Pyrenees. (d) Active Episyrphus migration (black dots on skyline) over the pass in October

FIGURE 2

Sample similarities and differential gene expression. (a) Principal component plot of the samples from nonmigrants (pink) and migrant (turquoise). (b) A heat map of the sample‐to‐sample distances and clustering of the samples. (c) Volcano plot of downregulated (blue), upregulated (red) and nonsignificant (grey) genes at a log2fold change of 1.5 and an adjusted p‐values of <.001

FIGURE 3

TreeMap of over represented GO process terms in the upregulated gene set. Each rectangle is a single cluster representative and is joined into “superclusters” of loosely related terms, visualized with different colours. The size of the rectangles reflects the enrichment p‐values

FIGURE 4

Differential gene expression in migrant Episyrphus. Genes appearing in the discussion and their assignment to functional categories along with expression calculated as log2fold change. Gene are placed within a theoretical framework for the genetic basis of migration depicting a cascade from environmental sensing, through hormonal control to down‐stream changes in migratory traits. Top: Environmental sensing of cues such as photoperiod, mediated by photosensitive proteins such as cry, modify circadian control of gene expression. IIS and circadian regulation converge on vri to modulate behavioural rhythms associated with migration such as flight and feeding. Middle: Hormonal control through IIS, JH, ecdysone pathways control reproductive diapause and longevity while also increasing energy stores and stress tolerance. Upregulation of octopamine (OA) synthesis pathways supply the high OA concentrations necessary for long periods of uninterrupted flight and the release of energy substrates into the haemolymph. A range of neuropeptide receptors and neuropeptides modulate flight, fuel, feeding and metabolic homeostasis. Bottom: Flight muscle proteins are upregulated and muscle function protected by autophagy via TGF‐β signalling and mitophagy through JAK/STAT signalling. The JAK/STAT pathway further contributes to immune protection from pathogens and stress responses, along with a range of other factors that protect the migrant from oxidative damage. Metabolism and fuelling genes highlight the role of lipid storage, activation and mobilisation for migration and the role of key limiting enzymes of the glycolytic pathway for regulating flight performance. Asterisk indicates genes previously identified as associated with migration in monarch butterflies. The genes foxo, fiz, EcR, Tdc1, Pdf, Akh, sNPF, dpp, put, Atg8a, Stat92E, CG4830 and CG17191 fall below 1.5 log2 fold change but within an adjusted p‐value of <.001 for differentially expressed genes. See discussion for details