Speciation microbiomes: consequences of gut bacteria on hybrid mortality in the genus Nasonia

Abstract

Symbiosis is a process by which two or more distinct organisms interact, whereas speciation is the diversifying process by which one species splits into two. Symbiosis and speciation are not commonly discussed together and can seem to be odd partners in their capacity to operate synergistically in nature. However, the complex community of microorganisms that live in symbiosis within an animal species—known as the microbiome—has the capacity to confer new traits and selective pressures that drive speciation. To demonstrate the microbiome’s influence in speciation, we present the following evidence using closely related insect species of the model Nasonia. First, the gut microbiome forms phylosymbiotic assemblages in which the relationships of the Nasonia-associated microbiomes parallel the evolutionary genetic relationships of Nasonia. Second, these phylosymbiotic assemblages become irregular in hybrids between the species. Third, the altered microbiome in hybrids is correlated with high rates of hybrid mortality. Fourth, when the hybrids are cured of their irregular microbiota, they are rescued from hybrid mortality. Finally, when the cured hybrids were reinoculated with bacteria, they recapitulated high rates of mortality. We conclude that in this animal complex, the gut microbiome is equally important as host genes in promoting hybrid mortality and thus advancing speciation.