Genetic Variation Predominates Over Developmental Temperature-Induced Plasticity in Shaping Migratory Flight Capacity...

Insects represent the largest group of migratory animals in terms of species and biomass, yet the relative contributions of population-associated genetic differentiation and environmental plasticity to insect migration remain unclear. Here, we integrate population genomics with common garden experiments to infer the geographic origins of immigrant populations and evaluate population- and developmental-temperature-associated variation in migration-related flight traits in the diamondback moth (Plutella xylostella), a major pest of cruciferous crops. Population-genomic analyses indicated that immigrant populations sampled in northern China were genetically most closely associated with southwestern populations, which were therefore considered inferred source populations, whereas southeastern populations showed limited genetic affinity with these immigrants and were treated as non-source reference populations. Genome scans identified 29 genes within outlier regions detected in comparisons of the immigrant and inferred source populations from the non-source reference populations; these genes were enriched for functions related to signal transduction and energy metabolism. Flight-mill assays under common garden conditions revealed that the immigrant and inferred source populations generally exhibited greater migration-associated flight capacity than the non-source reference populations. Individuals developing at lower temperatures also showed greater flight performance. Variance partitioning showed that population origin explained 15%-27% of the variation in flight-performance traits, whereas temperature explained 3%-7%. Genes located in population-genomic outlier regions did not overlap with temperature-responsive genes identified by RNA sequencing across developmental-temperature treatments in the immigrant population examined. Together, these findings show that population-associated differences persisting under common garden conditions accounted for more variation in migration-associated flight capacity than did the developmental-temperature treatments examined here.