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

Abstract

15Maintaining sexual reproduction in a highly competitive world is still one of the major mysteries 16 of biology given the apparently high efficiency of asexual reproduction. Co-evolutionary theories 17 such as the Red Queen hypothesis would suggest that the microbiomes in human reproductive 18 systems, specifically the microbiomes contained in semen and vaginal fluids, should reach some 19 level of homogeneity thanks to arguably the most conspicuous microbiome transmission between 20 two sexes. The long-term sexual coevolution should favor the dynamic homogeneity or stability, 21 which should also be beneficial for sexual reproduction such as sperm survival or fertilization on 22 physiological/ecological time scale. We present a piece of quantitative evidence in the form of 23 microbial community spatial heterogeneity to support the stability notion by analyzing three big 24 datasets of the human vaginal, semen and gut microbiome. Methodologically, we applied a 25 recent community-level extension to the classic Taylor's power law (Taylor 1961(Taylor , 1988: Nature), 26 which reached the rare status of ecological law and has found applications beyond biology. The 27 power law analysis revealed that human vaginal and semen microbiomes exhibited the same 28 scaling parameter size in their community spatial (inter-individual) heterogeneities, while both 29 exhibited significantly different heterogeneity scaling parameter with the human gut 30 microbiome. Both ecological and evolutionary theories, such as hologenome/holobiont and Red 31 Queen, even first principle, would predict that microbiome transmissions between two sexes 32 should have homogenizing effects on the composition and stability of the microbiomes in human 33 reproductive systems. 34 35 Running Head: Human reproductive system microbiomes 36 Keywords: Human gut microbiome; Human vaginal microbiome; Semen microbiome; 37 Heterogeneity; Power law extensions (PLEs); Red Queen theory; Hologenome 38 2 39 Importance 40 41Maintaining sexual reproduction in a highly competitive world is still one of the major mysteries 42 of biology given the apparently high efficiency of asexual reproduction. Co-evolutionary theories 43 such as the Red-Queen hypothesis would suggest that the microbiomes in human reproductive 44 systems, specifically the microbiomes contained in semen and vaginal fluids, should reach some 45 level of homogeneity thanks to arguably the most conspicuous microbiome transmission between 46 two sexes. The long-term sexual co-evolution should favor the dynamic homogeneity or stability, 47 which should also be beneficial for sexual reproduction such as sperm survival or fertilization on 48 physiological/ecological time scale. We present a piece of quantitative evidence in the form of 49 microbial community spatial heterogeneity to support the stability notion by analyzing three big 50 datasets of the human vaginal, semen and gut microbiome. Both ecological and evolutionary 51 theories would predict that microbiome transmissions between two sexes shou...

Microbiome Transmission During Sexual Intercourse Appears Stochastic and Supports the Red Queen Hypothesis

“…In spite of these apparently dramatic changes that occurred in vaginal microbiome after sexual intercourse, the relatively long term effects of the intercourse may be limited because of the resilience of normal vaginal microbiota ( Borovkova et al, 2011 ). In addition, the evolutionary implications of the microbiome transmission via sexual intercourse are still little known ( Ma and Taylor, 2020 ).…”

Spatial heterogeneity analysis of the human virome with Taylor’s power law

“…The term “heterogeneity” literally represents the quality or state of being diverse in character or content, which appears to be the other side of evenness coin or a proxy of biodiversity. However, much of the formal and quantitative research of heterogeneity in ecology has been performed separately from diversity research [14] , [15] , [17] , [18] . For instance, in population ecology, the terms such as heterogeneity, aggregation, dispersion, and patchiness are often used interchangeably, and all of which can be used to characterize the spatial distribution of biological populations.…”

“…At population scale, aggregation, dispersion and heterogeneity are often used interchangeably with each other, but the term aggregation is preferred. In population ecology, aggregation or heterogeneity is often measured quantitatively with Taylor’s [31] power law, which achieved rare status of ecological law [3] , [32] , [33] , [3] , [5] , [18] , [28] , [29] , [30] , [21] , [22] as further explained below shortly.…”

“…In addition, the heterogeneity of the assemblage of species, which falls between single-species population and community, can be measured with the so-termed mixed species population aggregation [11] . Several applications of the TPLE to human microbiome have been reported ( e.g ., [20] , [15] , [16] , [17] , [18] ). In the present study, we propose and test the application of TPLE for measuring the spatial heterogeneity of human virome.…”

Does Ulcerative Colitis Influence the Inter-individual Heterogeneity of the Human Intestinal Mucosal Microbiome?

“…Taylor’s power law (TPL) is a classic ecological model for assessing heterogeneity at the population scale 19 - 22 extended TPL from the population to the community level and introduced 4 types of power law extensions (Taylor’s power law extensions [TPLEs]), ie, Type-I to Type-IV TPLEs. 22 - 24 In this study, we aimed to answer the question of whether UC influences the spatial heterogeneity of human gut mucosal microbiome from both community and mixed-species levels by using Ma’s Type-I and Type-III TPLEs, respectively. The results of this study will hopefully generate important insights into the influence of UC on the gut mucosal microbiome.…”