Differences among populations and changes during domestication in the lipidome of Queensland fruit fly

As key components of insects' energy storage and mobilization systems and their various membranes, lipids are crucial to diverse phenotypes and fitness components of these metamorphic, poikilothermic organisms. Yet little is known about the ecological and evolutionary genetics of insect lipids. Historically, assay methodologies have been unable to resolve the diverse components of their lipidomes.

We have used modern lipidomics to screen for heritable differences in adult male Bactrocera tryoni, examining over 400 lipids in 15 different classes of neutral and phospho- ester and ether lipids. We found substantial differences in most classes between populations recently collected from opposite extremes of the species' range and/or during their subsequent domestication. Differences were found in both newly emerged and sexually mature flies. The differences in the former reflect differential use of resources accumulated in the larval stage during metamorphosis. The differences in the latter also reflect differential utilization of adult food resources. Most of the differences were found in the newly emerged flies and there was no obvious relationship between the differences at the two stages, implying largely independent genetic controls. The differences in lipid compositions seen among the recently collected strains suggest that lipids have played significant roles in ecotypic variation. In particular, differences in the acyl chain compositions of the phospholipids could have underpinned differences in the fluidity of the flies' membranes in the tropical versus temperate populations sampled. There were also many differences between the source populations in the patterns of change in their lipid profiles during domestication, suggesting they adapted in different ways to the 'common garden' laboratory environment; acyl chain compositions in lipids from the different populations converged, but their relative abundances did not.

The diverse patterns of genetic variation described here are consistent with the complex, multi-gene pathways for lipid syntheses and remodeling now being discovered by other insect 'omic' analyses and show that heritable lipid differences could underpin differences in a wide variety of adaptively important insect phenotypes.