The Impact of Symbiosis on Insect Behaviour and Speciation

Improving our knowledge on the biological processes and dynamics that cause speciation and biodiversity is a fundamental prerequisite for understanding evolutionary biology with broad implications on diverse biological fields such as ecology and medicine in the post-genomic area. Consequently, one of the most pivotal aims in evolutionary research is to determine and understand the mechanisms and internal and external factors that drive speciation in biological systems. Insects are the most diverse and rapidly evolving group of animals, with over a million of described species, more than half of all known living organisms on earth. Hence, in addition to their economical and medical implications, insects provide an exceptional model system for studying speciation mechanisms and dynamics. In face of recent progress in speciation research current standard models disregard the potential impact of microbial reproductive symbionts for driving host speciation. The maternally transmitted endosymbiont Wolbachia, for example, infects up to 76% of all insect species and is capable of manipulating host reproduction biology for its own benefit in many systems. The present proposal is aimed to survey systematically the temporal and spatial infection dynamics of Wolbachia and to monitor their phenotypic consequences on host fitness and sexual behavior in our tropical Drosophila speciation model system that is currently under incipient speciation.

Improving our knowledge on the biological processes and dynamics that cause speciation and biodiversity is a fundamental prerequisite for understanding evolutionary biology with broad implications on diverse biological fields such as ecology and medicine in the post-genomic area. Consequently, one of the most pivotal aims in evolutionary research is to determine and understand the mechanisms and internal and external factors that drive speciation in biological systems. Insects are the most diverse and rapidly evolving group of animals, with over a million of described species, more than half of all known living organisms on earth. Hence, in addition to their economical and medical implications, insects provide an exceptional model system for studying speciation mechanisms and dynamics. In face of recent progress in speciation research current standard models disregard the potential impact of microbial reproductive symbionts for driving host speciation. The maternally transmitted endosymbiont Wolbachia, for example, infects up to 76% of all insect species and is capable of manipulating host reproduction biology for its own benefit.This research project was aimed to survey systematically the temporal and spatial infection dynamics of Wolbachia and to monitor their phenotypic consequences on host fitness and sexual behavior in neotropical Drosophila speciation model system that is currently under incipient speciation. Here we found that in contrast to most other insect-Wolbachia symbioses, the endosymbiont is already a fixed and vital entity of the Drosophila host. Furthermore this obligate mutualist colonizes specifically the host germline in order to ensure its own vertical transmission, but also targets selectively defined somatic host tissues and organs, which are pivotal for sexual behavior: in males they occupy specific sex pheromone producing cells, the oenocytes, and in females they are found only in highly specialized brain regions that are functionally important for receiving and interpreting incoming pheromone signals expressed by males. In such the endosymbiont directs sexual mating behavior of their host in a sex-specific manner, since females that were depleted from Wolbachia can no longer distinguish between proper (compatible) and improper (incompatible) males, hereby risking severe fitness loss. In males, depletion of Wolbachia from oenocytes alters the profiles of male sex pheromones. Thereby, such males are no longer recognized as proper mates by native females and rejected. This study demonstrates how bacterial symbionts can affect and orchestrate mating behavior of both host sexes individually in an adaptive manner. Consequently, even slight perturbations of such intimate symbiotic interactions can easily trigger reproductive isolation, and upon genetic drift, even de novo speciation.