Human reproductive system microbiomes exhibited significantly different heterogeneity scaling with gut microbiome, but the intra-system scaling is invariant

Abstract

Maintaining sexual reproduction in a highly competitive world is still one of the major mysteries of biology given the apparently high efficiency of asexual reproduction. Co-evolutionary theories such as the Red Queen hypothesis would suggest that the microbiomes in human reproductive systems, specifically the microbiomes contained in semen and vaginal fluids, should reach some level of homogeneity thanks to arguably the most conspicuous microbiome transmission between two sexes. The long-term sexual coevolution should favor the dynamic homogeneity or stability, which should also be beneficial for sexual reproduction such as sperm survival or fertilization on physiological/ecological time scale. We present a piece of quantitative evidence in the form of microbial community spatial heterogeneity to support the stability notion by analyzing three big datasets of the human vaginal, semen and gut microbiome. Methodologically, we applied a recent community-level extension to the classic Taylors power law (Taylor 1961, 1988: Nature), which reached the rare status of ecological law and has found applications beyond biology. The power law analysis revealed that human vaginal and semen microbiomes exhibited the same scaling parameter size in their community spatial (inter-individual) heterogeneities, while both exhibited significantly different heterogeneity scaling parameter with the human gut microbiome. Both ecological and evolutionary theories, such as hologenome/holobiont and Red Queen, even first principle, would predict that microbiome transmissions between two sexes should have homogenizing effects on the composition and stability of the microbiomes in human reproductive systems.\n\nImportanceMaintaining sexual reproduction in a highly competitive world is still one of the major mysteries of biology given the apparently high efficiency of asexual reproduction. Co-evolutionary theories such as the Red-Queen hypothesis would suggest that the microbiomes in human reproductive systems, specifically the microbiomes contained in semen and vaginal fluids, should reach some level of homogeneity thanks to arguably the most conspicuous microbiome transmission between two sexes. The long-term sexual co-evolution should favor the dynamic homogeneity or stability, which should also be beneficial for sexual reproduction such as sperm survival or fertilization on physiological/ecological time scale. We present a piece of quantitative evidence in the form of microbial community spatial heterogeneity to support the stability notion by analyzing three big datasets of the human vaginal, semen and gut microbiome. Both ecological and evolutionary theories would predict that microbiome transmissions between two sexes should have homogenizing effects in human reproductive systems.