Natural and experimental speciation triggered by symbionts

Dramatic deprivation of biological diversity and global species extinction due to inconsiderate exploration of our natural resources and environment by recent humans are one of the main challenging problems of the 21th century. From a biological perspective however, evolutionary history has taught us that the vast majority of all species on this planet already got extinct, not due to human, but to natural selection. The antagonistic counterpart to extinction is speciation, a biological key process giving rise to diversification and the origin of newly adapted species. Although regarded as the central concept of evolutionary theory and hence under intensive studiy since Darwin, the entirety of their fundamental factors and exact mechanisms that trigger speciation per se are still not well understood. Insects are the most species-rich animal group on earth with more than 2-10 million estimated species, from which some like native American Drosophila are presently under speciation in nature. Having proven as a perfect experimental genetic and evolutionary model system since more than 100 years, Drosophila provides an ideal model also for deciphering the modalities and dynamics of the speciation process, not only retrospect but in real-time. In this project we propose to add a novel, currently mainly neglected, or at best vastly underestimated, speciation factor, i.e., symbotic microbes that universally coexist with their host species. Latest research has uncovered that all living organisms are super- organisms harboring trillions of microbes with beneficial or neutral functions. If not in balance with their host however, they can transform into pathogens. Some of them even live within host cells, called endosymbionts, which are with 70% global prevalence very common in insects, such as the maternally transmitted bacterium Wolbachia. This endosymbiont has recently attracted global interest when artificially transferred into disease-transmitting mosquitos by providing full biological protection via blocking other pathogens such as the Dengue virus. Impressively, Wolbachia can also manipulate host reproduction biology and, as we recently found in native American Drosophila, even host sexual behavior in favor of their own fitness and transmission success. Since bacteria have a much higher mutation rate than hosts and in cases where the host already is dependent on the presence of the beneficial microbe we propose that even slight perturbations of host-symbiont equilibria via external and/or internal stresses can trigger de novo host speciation even within short periods of time. We hence will test our hypothesis in natural and experimental systems of native American Drosophila species and follow their speciation dynamics and modalities at the phenotypic and genetical level. From this we expect to obtain a better understanding on the significance of symbionts to initiate speciation steps, how speciation works in nature and to provide a novel conceptual framework for possibly generating species diversity artificially.

Monitoring Natural and Experimental Speciation triggered by Endosymbionts Dramatic deprivation of biological diversity and global species extinction due to inconsiderate exploration of our natural resources and environment by recent humans are one of the main challenging problems of the 21th century. From a biological perspective however, evolutionary history has taught us that the vast majority of all species on this planet already got extinct, not due to human, but to natural selection. The antagonistic counterpart to extinction is speciation, a biological key process giving rise to diversification and the origin of newly adapted species. Although regarded as the central concept of evolutionary theory and hence under intensive study, the entirety of their fundamental factors and exact mechanisms that trigger speciation per se are still not well understood. Insects are the most species-rich animal group on earth with more than 2-10 million estimated species, from which some like native American Drosophila are presently under speciation in nature. Having proven as a perfect experimental genetic and evolutionary model system since more than 100 years, Drosophila provides an ideal model also for deciphering the modalities and dynamics of the speciation process, not only retrospect but in real-time. In this project we proposed to add a novel, currently mainly neglected, or at best vastly underestimated, speciation factor, i.e., symbiotic microbes that universally coexist with their host species. Latest research has uncovered that all living organisms are "super-organisms" harboring trillions of microbes with beneficial or neutral functions. If not in balance with their host however, they can transform into pathogens. Some of them even live within host cells, called endosymbionts, which are with 70% global prevalence very common in insects, such as the maternally transmitted bacterium Wolbachia. This endosymbiont has recently attracted global interest when artificially transferred into disease-transmitting mosquitos by providing full biological protection via blocking other pathogens such as the Dengue virus. Impressively, Wolbachia can also manipulate host reproduction biology and, as we recently found in native American Drosophila, even host sexual behavior in favor of their own fitness and transmission success. In this research project we found that Wolbachia (i) manipulate sexual behavior in both fly sexes by interfering with sexual hormone production and recognition, and (ii) can affect post-mating incompatibilities in very recently diverged subspecies under experimental conditions. We furthermore uncovered (iii) novel autophagy mechanisms restricting the bacteria already during early host embryogenesis to defined future body parts and unexpectedly (iv) a selfish mitochondrial genome that is transmitted by both parents and highly infective in these flies. Our novel and unexpected findings add to a better understanding on the significance of symbionts to initiate speciation steps and to provide a novel conceptual framework for possibly generating species diversity even artificially.