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.

High genetic connectivity of two pollinating flies despite urban disturbance

“…Hence, we wrongly predicted some level of IBD within study areas because our study species are not migratory. Given the high prevalence of hoverfly species presenting a partial migration syndrome (Doyle et al, 2022; Menz et al, 2019; Speight, 2017), the genetic and structural pathways to efficient dispersal might also be present in nonmigratory hoverflies such as SP and MF. Indeed, even rare nonmigratory species may fly several kilometers away from their emergence sites (Rotheray et al, 2014).…”

Evolution of tissue-specific expression of ancestral genes across vertebrates and insects

“…For other eight species, we downloaded GTF and genome FASTA files from Ensembl Metazoa [https://metazoa.ensembl.org/]: sea urchin ( Strongylocentrotus purpuratus: Spu: Spur_5.0 v51), fruit fly ( Drosophila melanogaster, Dme : dm6, v26), yellow fever mosquito ( Aedes aegypti, Aae : AaegL5, v46), domestic silk moth ( Bombyx mori, Bmo : ASM15162v1, v45), red flour beetle ( Tribolium castaneum, Tca : Tcas5.2, v45), honey bee ( Apis mellifera, Ame : Amel_4.5, v35), centipede ( Strigamia maritima , Sma: Smar1, v26), California two-spot octopus ( Octopus bimaculoides, Obi : ASM119413v2). For other three species, we used the GTF and genome FASTA files from the relative publications: amphioxus ( Branchiostoma lanceolatum , Bla: 54 ), marmalade hoverfly ( Episyrphus balteatus , Eba: 55 ), mayfly ( Cloeon dipterum , Cdi: 12 ). For the cockroach ( Blattella germanica , Bge) we downloaded the GFF3 (blager_OGSv1.2.1.gff3) and the genome FASTA (GCA_000762945.2_Bger_2.0_genomic.fna.gz) from https://i5k.nal.usda.gov/content/data-downloads.…”

Rapid evolutionary change, constraints and the maintenance of polymorphism in natural populations of Drosophila melanogaster

“…The fezzik ( fiz ) gene is located on the X chromosome and its expression has been shown to affect a variety of traits, including larval growth rate, body size determination, cold and insecticide tolerance (Glaser‐Schmitt & Parsch, 2018). In a study using replicate experimental populations of D. melanogaster , fiz was strongly down‐regulated in populations adapted to larval malnutrition (Kawecki et al, 2021); while another study detected its orthologue as highly up‐regulated in actively migrating Episyrphus balteatus in comparison to the non‐migratory summer morph (Doyle et al, 2022). The fiz protein shows evidence for adaptive protein evolution since D. melanogaster 's divergence from D. simulans (Langley et al, 2012; Saminadin‐Peter et al, 2012), with fiz ranked among the top candidates for adaptive evolution on the D. melanogaster lineage (Langley et al, 2012).…”

“…In line with this observation, previous work found that fiz expression affects adult starvation resistance in a sex‐specific manner, and that in the genetic background of a natural population, variation at SNP67 has a stronger effect in females than in males (Glaser‐Schmitt et al, 2021), suggesting that adult starvation resistance may be the phenotype under selection. However, it is possible that a combination of it and/or other traits that fiz expression has been proposed or demonstrated to affect (see Glaser‐Schmitt & Parsch, 2018; Kawecki et al, 2021; Doyle et al, 2022 for examples) are the target(s) of selection. Similarly, it is important to note that there are many factors relevant to selection in nature that are not accounted for in the models we considered.…”

“…that fiz expression has been proposed or demonstrated to affect (seeGlaser-Schmitt & Parsch, 2018;Kawecki et al, 2021;Doyle et al, 2022 for examples) are the target(s) of selection. Similarly, it is important to note that there are many factors relevant to selection in nature that are not accounted for in the models we considered.…”