Phenotypic disruption of cuticular hydrocarbon production in hybrids between sympatric species of Hawaiian picture-wing Drosophila (original) (raw)

Interspecies hybrids can express phenotypic traits far outside the range of parental species. The atypical traits of hybrids provide insight into differences in the factors that regulate the expression of these traits in the parental species. In some cases, the unusual phenotypic traits of hybrids can lead to phenotypic dysfunction with hybrids experiencing reduced survival or reproduction. Cuticular hydrocarbons (CHCs) in insects are important phenotypic traits that serve several functions, including desiccation resistance and pheromones for mating. We used gas chromatography mass spectrometry to investigate the differences in CHC production between two closely related sympatric Hawaiian picture-wing Drosophila species, Drosophila heteroneura and D. silvestris, and their F1 and backcross hybrid offspring. CHC profiles differed between males of the two species, with substantial sexual dimorphism in D. silvestris but limited sexual dimorphism in D. heteroneura. Surprisingly, F1 hybrids did not produce three CHCs, and the abundances of several other CHCs occurred outside the ranges present in the two parental species. Backcross hybrids produced all CHCs with greater variation than observed in F1 or parental species. Overall, these results suggest that the production of CHCs was disrupted in F1 and backcross hybrids, which may have important consequences for their survival or reproduction. Interspecies hybrids that express phenotypic traits far outside the range present in the parental species can provide insights into the factors that regulate the expression of these traits 1. These unusual phenotypic traits in hybrids can also reflect a type of phenotypic dysfunction in which hybrid individuals experience reduced survival or reproduction 2,3. Several types of gene interactions may be involved in hybrid disruption, such as cis-trans regulation or post-transcriptional processes, including mRNA splicing and processing 4,5. Further, translational alterations resulting in changed amino acids may result in proteins incapable of interacting, thus producing less-fit hybrid phenotypes 6. Cuticular hydrocarbons (CHCs) are abundant components of insect cuticles 7,8 that are produced through complex biochemical processes 9,10 and involve the interaction of genes on different chromosomes 11. CHCs display a wide range of distinct compounds that vary across insect taxa and occur as a complex mixture of hydrophobic linear, branched, saturated, and unsaturated compounds 11-13. CHCs are known to act as pheromones and influence a wide variety of behaviors, including courtship, mate discrimination, learning, aggregation, and dominance 5,8,14 , and they have a strong influence on individual fitness, helping insects to resist starvation 15 , tolerate extreme environments 16 , and prevent desiccation 17-19. In D. melanogaster, the alteration or disruption of genes involved in CHC biosynthesis can result in the complete absence 20 or overproduction 21 of CHCs, changes that have the potential to negatively impact mating, copulation behavior, and survivability 10,22 .