Genetic variance and phenotypic selection on pathogen-linked oviposition choice in Drosophila

Pathogen-avoidance behaviour is assumed to be adaptive, yet its phenotypic variability and genetic heritability are rarely quantified. In species lacking post-oviposition care, avoiding potentially infectious egg-laying substrates would improve offspring survival and should therefore be under strong selection. We used two-choice oviposition assays to quantify the phenotypic and genetic variance in, and the fitness consequences of, oviposition preference in Drosophila melanogaster when exposed to egg-laying substrates containing the pathogenic bacterium Pseudomonas aeruginosa PA14. Oviposition preference varied substantially in an outbred population and was bimodal: many females laid all eggs on the bacterial substrate or all on the clean substrate. Across all choice assays, more eggs and more viable offspring were produced on the bacterial surface, with no overall difference in egg-to-adult viability between substrates. Among extreme phenotypes, females laying exclusively on bacteria laid more eggs but had lower egg-to-adult viability than those laying exclusively on clean food, resulting in similar numbers of adult offspring. The broad sense heritability of oviposition preference, measured in 24 inbred fly lines, was moderate (H2 = 0.30). Selection analyses indicated opposing selection acting on oviposition preference via different fitness components, with balancing acting via egg number and positive directional selection for avoidance acting via egg-to-adult viability. Such opposing effects may reflect a trade-off females face between avoiding high density oviposition sites, while also avoiding potential pathogenic effects on egg development.