Development of mating preference is considered to be an early event in speciation. In this study, mating preference was achieved by dividing a population of Drosophila melanogaster and rearing one part on a molasses medium and the other on a starch medium. When the isolated populations were mixed, “molasses flies” preferred to mate with other molasses flies and “starch flies” preferred to mate with other starch flies. The mating preference appeared after only one generation and was maintained for at least 37 generations. Antibiotic treatment abolished mating preference, suggesting that the fly microbiota was responsible for the phenomenon. This was confirmed by infection experiments with microbiota obtained from the fly media (before antibiotic treatment) as well as with a mixed culture of Lactobacillus species and a pure culture of Lactobacillus plantarum isolated from starch flies. Analytical data suggest that symbiotic bacteria can influence mating preference by changing the levels of cuticular hydrocarbon sex pheromones. The results are discussed within the framework of the hologenome theory of evolution.

Summary: Emerging diseases have been responsible for the death of about 30% of corals worldwide during the last 30 years. Coral biologists have predicted that by 2050 most of the world's coral reefs will be destroyed. This prediction is based on the assumption that corals can not adapt rapidly enough to environmental stress‐related conditions and emerging diseases. Our recent studies of the Vibrio shiloi/Oculina patagonica model system of the coral bleaching disease indicate that corals can indeed adapt rapidly to changing environmental conditions by altering their population of symbiotic bacteria. These studies have led us to propose the Coral Probiotic Hypothesis. This hypothesis posits that a dynamic relationship exists between symbiotic microorganisms and environmental conditions which brings about the selection of the most advantageous coral holobiont. Changing their microbial partners would allow the corals to adapt to changing environmental conditions more rapidly (days to weeks) than via mutation and selection (many years). An important outcome of the Probiotic Hypothesis would be development of resistance of the coral holobiont to diseases. The following evidence supports this hypothesis: (i) Corals contain a large and diverse bacterial population associated with their mucus and tissues; (ii) the coral‐associated bacterial population undergoes a rapid change when environmental conditions are altered; and (iii) although lacking an adaptive immune system (no antibodies), corals can develop resistance to pathogens. The Coral Probiotic Hypothesis may help explain the evolutionary success of corals and moderate the predictions of their demise.

The holobiont (host with its endocellular and extracellular microbiome) can function as a distinct biological entity, an additional organismal level to the ones previously considered, on which natural selection operates. The holobiont can function as a whole: anatomically, metabolically, immunologically, developmentally, and during evolution. Consideration of the holobiont with its hologenome as an independent level of selection in evolution has led to a better understanding of underappreciated modes of genetic variation and evolution. The hologenome is comprised of two complimentary parts: host and microbiome genomes. Changes in either genome can result in variations that can be selected for or against. The host genome is highly conserved, and genetic changes within it occur slowly, whereas the microbiome genome is dynamic and can change rapidly in response to the environment by increasing or reducing particular microbes, by acquisition of novel microbes, by horizontal gene transfer, and by mutation. Recent experiments showing that microbiota can play an initial role in speciation have been suggested as an additional mode of enhancing evolution. Some of the genetic variations can be transferred to offspring by a variety of mechanisms. Strain-specific DNA analysis has shown that at least some of the microbiota can be maintained across hundreds of thousands of host generations, implying the existence of a microbial core. We argue that rapid changes in the microbiome genome could allow holobionts to adapt and survive under changing environmental conditions thus providing the time necessary for the host genome to adapt and evolve. As Darwin wrote, “It is not the strongest of the species that survives but the most adaptable”.

The hologenome concept of evolution postulates that the holobiont (host plus symbionts) with its hologenome (host genome plus microbiome) is a level of selection in evolution. Multicellular organisms can no longer be considered individuals by the classical definitions of the term. Every natural animal and plant is a holobiont consisting of the host and diverse symbiotic microbes and viruses. Microbial symbionts can be transmitted from parent to offspring by a variety of methods, including via cytoplasmic inheritance, coprophagy, direct contact during and after birth, and the environment. A large number of studies have demonstrated that these symbionts contribute to the anatomy, physiology, development, innate and adaptive immunity, and behavior and finally also to genetic variation and to the origin and evolution of species. Acquisition of microbes and microbial genes is a powerful mechanism for driving the evolution of complexity. Evolution proceeds both via cooperation and competition, working in parallel.