DOCSLIB.ORG

The Hologenome Concept of Evolution: Medical Implications

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
The Hologenome Concept of Evolution: Medical Implications Open Access Rambam Maimonides Medical Journal REVIEW ARTICLE The Hologenome Concept of Evolution: Medical Implications Eugene Rosenberg, Ph.D.* and Ilana Zilber-Rosenberg, Ph.D. Department of Molecular Microbiology and Biotechnology, Tel Aviv University, Ramat Aviv, Israel ABSTRACT All natural animals and plants are holobionts, consisting of the host and microbiome, which is composed of abundant and diverse microorganisms. Health and disease of holobionts depend as much on interactions between host and microbiome and within the microbiome, as on interactions between organs and body parts of the host. Recent evidence indicates that a significant fraction of the microbiome is transferred by a variety of mechanisms from parent to offspring for many generations. Genetic variation in holobionts can occur in the microbiome as well as in the host genome, and it occurs more rapidly and by more mechanisms in genomes of microbiomes than in host genomes (e.g. via acquisition of novel microbes and horizontal gene transfer of microbial genes into host chromosomes). Evidence discussed in this review supports the concept that holobionts with their hologenomes can be considered levels of selection in evolution. Though changes in the microbiome can lead to evolution of the holobiont, it can also lead to dysbiosis and diseases (e.g. obesity, diarrhea, inflammatory bowel disease, and autism). In practice, the possibility of manipulating microbiomes offers the potential to prevent and cure diseases. KEY WORDS: Beneficial microbes, genetic variation, holobiont, hologenome, microbiome INTRODUCTION Biology is undergoing a paradigm change. Animals tween microorganisms and animals/plants, once and plants can no longer be considered individuals.1 thought to be rare events, are actually a hallmark of All are holobionts, consisting of the host and abun- eukaryotic life. dant and diverse microbiotas, which comprise bac- A decade ago, we published the hologenome con- teria, archaea, viruses, and protists. Symbioses be- cept of evolution, which posits that the holobiont, in Abbreviations: ASDs, autism spectrum disorders; CD, Crohn’s disease; IBD, inflammatory bowel disease; FMT, fecal microbiota transplantation. Citation: Rosenberg E, Zilber-Rosenberg I. The Hologenome Concept of Evolution: Medical Implications. Rambam Maimonides Med J 2019;10 (1):e0005. Review. doi:10.5041/RMMJ.10359 Copyright: © 2019 Rosenberg and Zilber-Rosenberg. This is an open-access article. All its content, except where otherwise noted, is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Conflict of interest: No potential conflict of interest relevant to this article was reported. * To whom correspondence should be addressed. E-mail: [email protected] Rambam Maimonides Med J | www.rmmj.org.il 1 January 2019 Volume 10 Issue 1 e0005 The Hologenome Concept concert with its hologenome, is a level of selection in THE HOLOGENOME CONCEPT OF evolution.2,3 Considerable data have accumulated EVOLUTION since the concept was first proposed that support The hologenome concept of evolution is based on and enrich it.4 Much of the data have come from the four generalizations: development of DNA-based techniques for analyzing bacterial communities, without having to culture 1. All natural animals and plants are holobionts them. containing abundant and diverse microbiota. As soon as the right method was found, 2. Holobionts can function as distinct biological discoveries came as easily as ripe apples from entities, anatomically, metabolically, immuno- a tree. (Robert Koch, 1905 Nobel Prize logically, during development and in evolution. Laureate in Physiology or Medicine) Microbiomes participate in achieving fitness of the holobionts. Though there have been a number of recent reviews on the role of the microbiome in human 3. A significant fraction of the microbiome genome health and disease,5–10 in this review we wish to together with the host genome is transmitted briefly describe the hologenome concept and discuss from one generation to the next, and thus can how it offers new perspectives to modern medicine. propagate unique properties of the holobiont. 4. Genetic variation in holobionts can occur by changes in the host and/or microbiome ge- nomes. Since the microbiome genome can adjust Box A. Definitions to environmental dynamics more rapidly and by Bacterial species: the most widely used bacterial more processes than the host genome, it can play species definition is a group of strains showing a fundamental role in adaptation and evolution over 97% of 16S rDNA gene-sequence identity. of holobionts. Holobiont: a term introduced by Margulis,11 which now refers to the host plus the entire microbiome. Plants, Animals, and Humans are Hologenome: the union of all the genes in a Holobionts holobiont, i.e. the host genome plus all of the Development of non-culturing, DNA-based methods genomes of the microbiome.3 for analyzing bacterial communities has led to the Horizontal gene transfer (HGT): transfer of determination of bacterial species diversity in a wide groups of genes between bacteria of different taxa assortment of non-vertebrates, vertebrates, and and from microbiomes to their hosts. plants. It is now clear that all natural animals and Horizontal transmission of microbiota: transfer plants contain hundreds or thousands of different of microorganisms from parent to offspring via the bacterial species as well as abundant viruses14 and environment. often fungi15; the two last-mentioned have not been studied extensively to date. For example, it has been Microbiome: the community of symbiotic microorganisms.12 reported that the human gut contains 5,700 bacte- rial species,16 and human skin contains 1,000 spe- Microbiota: microorganisms in the microbiome, cies.17 These are minimum numbers since rare but not necessarily all of it. species cannot be determined by current methods. Symbiosis: the term was first coined by Anton de Because of the large diversity of bacterial species, Bary in the mid-nineteenth century as “the living the gut microbiome contains ca. 9 million unique 3(p.276) together of different species.” This broad protein-coding genes or 400 times more bacterial definition is generally accepted, and easily comes 18 to terms with the hologenome concept. The genes than human genes. symbiotic system is usually constructed from a One of the unexpected findings of studies of gut large partner termed the host and smaller partners microbiomes is the enormous variation between in- called symbionts. A symbiont can be mutualistic, commensal, or pathogenic. dividual humans; the bacterial species composition within the human gut is unique to each person. Nev- Vertical transmission of microbiota: transfer ertheless, microbiomes of different individuals are from parent to offspring without mixing with closer to each other than to microbiomes of other microorganisms from the environment.13 primates,19 suggesting that there is something com- Rambam Maimonides Medical Journal 2 January 2019 Volume 10 Issue 1 e0005 The Hologenome Concept mon (a core) to the human microbiome. Shapira20 Microbiomes Affect the Fitness of has discussed the differences between conserved Holobionts core microbiota and flexible, environmentally driven A large number of studies have demonstrated the microbiota, with regard to their maintenance and beneficial interactions between microbiomes and contributions to host adaptation. It should be em- their hosts, leading to a better-adapted holobiont. phasized that “presence” or “absence” of a bacterial Table 1 summarizes major contributions of the species depends on technical limits of detection. microbiome to holobionts. Methods developed to detect rare species may reveal that there are many more common (core) species A large number of studies have shown that than currently considered and that individual varia- resident microbes protect holobionts from patho- tion may be the result of quantitative rather than gens. For example, following oral infection, the qualitative differences that are caused by a different numbers of Listeria monocytogenes were 10,000- diet or other environmental factors. Foods, such as fold higher in the small intestine of germfree (GF) red wine,21 tea, coffee,22 and chocolate,23 food addi- mice compared to conventional (CV) mice.37 Also tives, such as food emulsifiers24 and artificial sweet- Staphylococcus aureus infection is prevented by eners,25 and essentially any material that is put in resident Corynebacterium species.38 Blocking bind- the mouth affect the gut microbiome at all ages. ing sites and production of antibiotics are two com- Also, microbiomes are affected by physical activity26 mon mechanisms by which resident bacteria protect and illnesses, e.g. cancer27 and diabetes.28 Clearly, the holobiont against pathogens.39,40 A strong argu- the complexity and dynamics of microbiomes are ment for the role of bacteria in combatting infec- only beginning to be appreciated. tious disease is the successful treatment of patients, suffering from severe diarrhea caused by Clostridi- Microbiomes change also with age. Newborns are um difficile infection, with fecal transplants from dominated by facultative anaerobes such as the Pro- healthy donors (see further on).41 teobacteria, after which the diversity of strict anaer- obes within the Firmicutes and Bacteroidetes
Load more

Recommended publications
  • Holobionts As Units of Selection and a Model of Their Population Dynamics and Evolution
    Biological Theory https://doi.org/10.1007/s13752-017-0287-1 ORIGINAL ARTICLE Holobionts as Units of Selection and a Model of Their Population Dynamics and Evolution Joan Roughgarden1,6 · Scott F. Gilbert2 · Eugene Rosenberg3 · Ilana Zilber‑Rosenberg4 · Elisabeth A. Lloyd5 Received: 15 January 2017 / Accepted: 5 September 2017 © Konrad Lorenz Institute for Evolution and Cognition Research 2017 Abstract Holobionts, consisting of a host and diverse microbial symbionts, function as distinct biological entities anatomically, metabolically, immunologically, and developmentally. Symbionts can be transmitted from parent to offspring by a variety of vertical and horizontal methods. Holobionts can be considered levels of selection in evolution because they are well- defined interactors, replicators/reproducers, and manifestors of adaptation. An initial mathematical model is presented to help understand how holobionts evolve. The model offered combines the processes of horizontal symbiont transfer, within-host symbiont proliferation, vertical symbiont transmission, and holobiont selection. The model offers equations for the popula- tion dynamics and evolution of holobionts whose hologenomes differ in gene copy number, not in allelic or loci identity. The model may readily be extended to include variation among holobionts in the gene identities of both symbionts and host. Keywords Holobiont · Holobiont model · Hologenome · Level of selection · Microbiome · Microbiota · Symbiont Introduction also provides a model for the evolution of a holobiont that combines microbe and host population processes. This article discusses the concept of a holobiont—an ani- Following Lederberg and McCray (2001), a microbiome mal or plant host together with all the microbes living on or refers to an “ecological community of commensal, symbi- in it, exosymbionts and endosymbionts, respectively.
    [Show full text]
  • The Hologenome Concept of Evolution After 10 Years Eugene Rosenberg* and Ilana Zilber-Rosenberg
    Rosenberg and Zilber-Rosenberg Microbiome (2018) 6:78 https://doi.org/10.1186/s40168-018-0457-9 REVIEW Open Access The hologenome concept of evolution after 10 years Eugene Rosenberg* and Ilana Zilber-Rosenberg Abstract 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.
    [Show full text]
  • The NIH Catalyst from the Deputy Director for Intramural Research
    Fostering Communication and Collaboration The nihCatalyst A Publication for NIH Intramural Scientists National Institutes of Health Office of the Director Volume 4, Issue 4 July-August 1996 MCL, Moving Forward, Charge! Safety and Science Card Project Goes NIH-Wide Forward in Tandem by Celia Hooper and Rebecca Kolberg by Rebecca Kolberg slim piece of plastic and a little Immunological Genetics Section of NCH- shopping savvy is all it took to save GR’s Laboratory of Gene Transfer a quar- an NCHGR lab more than $250,000. ter-million dollars with her smart use of the mproving safety and improving ease A that a act to fol- I of scientific research are not neces- Although may be tough charge card. In the pre-card era, the lab of NIH’s charge-card sarily mutually exclusive. Proof of that low, the expansion bought the recombinant interleukin-2 will soon give hundreds more (IL-2) it cells has just arrived on the south edge of program that uses to culture T from scientists their the NIH campus in the form of a newly intramural Life Technologies Inc. in to save time renovated facility for research involving own chance Gaithersburg, Md., at a cost and, possibly, big bucks. of about $250,000 a year. pathogens that demand the highest lev- “I THINK THE REAL the basis of the els of containment. On Now, armed with an NIH results of a 30-card pilot pro- and a prescrip- Although the new Maximum Con- VALUE OF THE CARDS charge-card at and NCI, written an M.D., tainment Laboratory (MCL) is located in gram NCHGR tion by NIH is moving ahead and Pepper went to Giant Dis- the same space as NIH’s old Biosafety IS IN THE TIME offering all institutes, centers, Level-4 (BL-4) facility in Building 41 A, count Pharmacy and bought and divisions (ICDs) the year’s supply of IL-2 for the difference between the old and new SAVED—TIME SAVED a opportunity to allow their re- facilities extends far beyond a simple $2,490—saving a cool searchers to apply for their $247,510.
    [Show full text]
  • Dream World Under the Sea / Big Dreams for Small Creatures
    Big Dreams for Small Creatures: Ilana and Eugene Rosenberg's path to the Hologenome Theory Ehud Lamm "How did the idea originate? My bugs were not doing what they were supposed to". That's Eugene Rosenberg, eighty years old, idiosyncratic, cigar-smoking, English speaking, American-born Israeli microbiologist hailing from Tel Aviv, explaining what prompted him and his wife Ilana to rethink evolution, ecology and what it means to be an individual. What started as an empirical investigation into how corals respond to changing sea temperature eventually led the Rosenbergs to the claim that bacteria are integral parts of evolving individuals, far from their typical portrayal as pathogens. Indeed, they and their colleagues have further suggested that by altering organisms’ mate choice, symbiotic bacteria are an important factor in the origin of new species, and that their mechanisms for cell-to-cell adhesion and signaling render them strong candidates for having paved the way to multicellular organisms. Symbiosis with bacteria, so it would seem, is crucial to understanding both evolution and the self.1 Along the way, so I will claim, the Rosenbergs are nudging us beyond seeing the individual organism, for example each of us, as something with clear boundaries. Rather, individuals are similar to clouds, sharing and exchanging water droplets with nearby billows and with the environment, the droplets being bacteria. Individuals in this picture are multi-species consortiums. If this pulsating picture of the living world is true, the boundary lines between evolutionary change and ecological change will have to be redrawn. Eugene Rosenberg is a biochemist.
    [Show full text]
  • Coral Microbiology , Volume 2, a Quarterly 20, Number the O Journal of by Eugene Rosenberg, Christina A
    This article has This been published in or collective redistirbution of any portion of this article by photocopy machine, reposting, or other means is permitted only with the approval of The approval portionthe ofwith any permitted articleonly photocopy by is of machine, reposting, this means or collective or other redistirbution A S E A O F M I cr OB E S > SecTION V. EX AMPLES OF DIverSITY > CHAPTer 10. MIcrOBIAL COmmUNITIES Oceanography > C. COR AL Reef MIcrOBIOLOGY Coral Microbiology journal of The 20, Number 2, a quarterly , Volume BY EUGene ROSenBerG, CHRISTINA A . KELLOGG, AND FOreST ROHWer In the last 30 years, there has been their effects by altering the microbial tains multiple “taxa” (Baker, 2003). A approximately a 30% loss of corals population and causing certain microbes single species of coral can host multiple O worldwide, largely due to emerging dis- to become pathogens. types of Symbiodinium, often contain- ceanography eases (Harvell et al., 2002, 2007; Hughes ing different clades at different depths et al., 2003). Coral microbiology is a new MIcrOORGANISMS ASSOCIATED (Rowan and Knowlton, 1995). Reviews S ociety. Copyright 2007 by The 2007 by Copyright ociety. field, driven largely by a desire to under- WITH HeALTHY CORALS of Symbiodinium diversity, systematics, stand the interactions between corals The coral holobiont (host organism plus and relationships to coral diseases are and their symbiotic microorganisms and all of its associated microorganisms) is presented by Baker (2003, 2004). to use this knowledge to eventually pre- a complex system containing microbial vent the spread of coral diseases. representatives of all three domains: Bacteria O ceanography ceanography The last decade has brought substan- Eucarya, Bacteria, and Archaea, as well Corals provide three general habitats for O ceanography ceanography tial progress in determining the abun- as numerous viruses (Figure 1).
    [Show full text]
  • The Human Microbiome, Social Phenomena and the Hologenome
    discip ter lina OPEN ACCESS Freely available online In ry f o S l o a c n i a r l u S o c J i l e a n b c e o Global Journal of Interdisciplinary Social Sciences l s G ISSN: 2319-8834 Research Article The human microbiome, social phenomena and the hologenome concept of evolution Eugene Rosenberg Department of Molecular Microbiology and Biotechnology, Tel Aviv University, Ramat Aviv, Givat Shmuel, Israel. ABSTRACT The recently developed hologenome concept of evolution posits that all plants and animals, Including humans are holobionts, consisting of a host and diverse symbiotic microorganisms, Termed the microbiome, acting in numerous ways as a single unit. This article offers an initial consideration of how this concept can add a different perspective to the understanding of three social issues. (a) Mother`s microbiome influences offspring`s health and social standing. (b) Cooperation, going hand in hand with competition, occurs at all levels, from cells to organisms to societies. (c) The microbiome, that can store and express acquired information between generations, is a possible mechanism for understanding collective memory. Keywords: hologenome, holobiont, microbiome, evolution, social darwinism, collective memory, unconscious memory, motherhood INTRODUCTION recent developments in social neuroscience, cultural Three recent articles have discussed the relevance of biology and behavioral epigenetics that support early biological theory to sociology (Nichols 2020). One ideas proposed independently by George Herbert Mead article traces the history of evolutionary thinking in (1863-1931) and Norbert Elias (1897-1990). Shalin sociology, its rise, demise and recent resurrection (Schutt argues that both authors accepted Darwin’s view that and Turner 2019).
    [Show full text]
  • Eugene Rosenberg Current Knowledge and Unanswered Questions
    The Microbiomes of Humans, Animals, Plants, and the Environment 2 Eugene Rosenberg Microbiomes Current Knowledge and Unanswered Questions The Microbiomes of Humans, Animals, Plants, and the Environment Volume 2 This series covers microbiome topics from all natural habitats. Microbiome research is a vibrant field of science that offers a new perspective on Microbiology with a more comprehensive view on different microorganisms (microbiota) living and working together as a community (microbiome). Even though microbial communities in the environment have long been examined, this scientific movement also follows the increasing interest in microbiomes from humans, animals and plants. First and foremost, microbiome research tries to unravel how individual species within the community influence and communicate with each other. Addi- tionally, scientists explore the delicate relationship between a microbiome and its habitat, as small changes in either, can have a profound impact on the other. With individual research volumes, this series reflects the vast diversity of Microbiomes and highlights the impact of this field in Microbiology. More information about this series at http://www.springer.com/series/16462 Eugene Rosenberg Microbiomes Current Knowledge and Unanswered Questions Eugene Rosenberg Department of Molecular Microbiology & Biotechnology Tel Aviv University Givat Shmuel, Tel Aviv, Israel ISSN 2662-611X ISSN 2662-6128 (electronic) The Microbiomes of Humans, Animals, Plants, and the Environment ISBN 978-3-030-65316-3 ISBN 978-3-030-65317-0
    [Show full text]
  • Prebiotics and Probiotics Within the Framework of the Hologenome Concept
    & Bioch ial em b ic Zilber-Rosenberg and Rosenberg J Microbial Biochem Technol 2011, S1 ro a c l i T M e DOI: 10.4172/1948-5948.S1-001 f c h o Journal of n l o a n l o r g u y o J ISSN: 1948-5948 Microbial & Biochemical Technology ReviewResearch Article Article OpenOpen Access Access Prebiotics and Probiotics within the Framework of the Hologenome Concept Ilana Zilber-Rosenberg1 and Eugene Rosenberg2* 1Independent scholar, Rahavat Ilan St., Givat Shmuel, Israel 2Department of Molecular Microbiology & Biotechnology, Tel Aviv University, Ramat Aviv, 69978, Israel Abstract Prebiotics and probiotics fall within the framework of the hologenome concept which posits that the holobiont (host plus all of its associated microorganisms) with its hologenome, acting in consortium affects all aspects of the holobiont’s fitness (adaptation, survival, development, growth and reproduction) and evolution. Variation in the holobiont can be brought about by amplification of endogenous microbes and by acquision of novel strains. Prebiotics and probiotics function by these mechanisms and can cause rapid changes in the diverse microbiota, which not only can benefit (or harm) the holobiont in the short term but also can be transmitted to offspring and lead to long lasting cooperations and changes which cannot as yet be predicted. The role of bacteriophages in moderating the effects of prebiotics and probiotics is also discussed. Keywords: Prebiotic; Probiotic; Hologenome; Holobiont; Symbiosis; symbiotic microbiota [9]. and the hologenome is the sum of the genetic Bacteriophage information of the host and its microbiota. The theory is based on four generalizations, each of which is supported by a large body of empirical Introduction data: Interest in the natural microbiota and claims of its advantage to (i) All animals and plants harbor abundant and diverse human health paralleled the development of microbiological research microorganisms.
    [Show full text]
  • Cdhc Coral Disease
    CORAL DISEASE AND HEALTH: A NATIONAL RESEARCH PLAN National Oceanic and Atmospheric Administration In Cooperation with Federal, State, Academic, Non-profit Marine Laboratories and Industry Partners September, 2003 About This Document Editors’ Acknowledgements - This document was prepared and printed with support from NOAA through the Coral Conservation Program and the Living Oceans Foundation. Layout and design was provided by Andrew Bruckner, NOAA Fisheries. Sylvia Galloway and Cheryl Woodley, NOAA CCEHBR and Andrew Bruckner, NOAA Fisheries compiled working group reports and provided technical edits. Photo Credits- Images were provided by: Biscayne National Park - Richard Curry; FDA - Sherry Curtis; Hawaii Institute of Marine Biology - Teresa Lewis; Johns Hopkins University - Gary Ostrander; Medical Univ. of South Carolina - Sara Polson, Shawn Polson; NOAA AOML, Miami - Monica Gurnee, Jim Hendee; NOAA CCEHBR, Charleston - John Bemiss, Marie DeLorenzo, Cheryl Woodley, Darren Wray; NOAA CCEHBR, Oxford - Dorothy Howard, Shawn McLaughlin, Kathy Price; NOAA Fisheries, Miami - Charles Fasano; NOAA Fisheries, Silver Spring, - Andy Bruckner; NOAA, NESDIS, Silver Spring - Gang Lui, Al Strong; Tel Aviv Univ. - Eugene Rosenberg; TetraTech - Esther Peters; USGS - Paul Mendenwaldt, Thierry Work; Virgin Islands National Park - Jeff Miller; Waikiki Aquarium, Univ. Hawaii, Manoa - Cindy Hunter. Cover Photos: Montastraea faveolata with white plague, Bonaire, 2001 (photo by Andrew Bruckner); diver surveying M. annularis for white plague in Virgin Islands National Park (photo by Jeff Miller); coral tissue destruction by algal turf on the skeleton of a colony of Stephanocoenia intersepta. Stained with Harris's hematoxylin and eosin (photomicrograph by Esther Peters). Back page: Red-band disease on a sea fan; white-band disease on Acropora palmata; partially bleached Diploria labyrinthiformis; dark-spots disease on Siderastrea siderea; yellow-blotch disease on Montastraea faveolata; spot biting by Sparisoma viride on M.
    [Show full text]
  • Holobiont Evolution: Model with Lineal Vs
    bioRxiv preprint doi: https://doi.org/10.1101/465310; this version posted December 12, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY 4.0 International license. Holobiont Evolution: Model with Lineal vs. Collective Hologenome Inheritance 1,2 Joan Roughgarden ⇤ 1Department of Biology, Stanford University, Stanford CA 94305, USA 2Hawaii Institute of Marine Biology, University of Hawaii, Kaneohe HI 96744, USA ⇤To whom correspondence should be addressed; E-mail: [email protected]. The intimate integration of microbiomes with their hosts might imply that the holobiont is a unit of evolution and that selection on holobionts is an important evolutionary force. Skeptics argue that vertical transmission of microbes is too uncommon for holobiont selection to be evolutionarily important. What has been missing is a simple mathematical model to assess how holobiont selection may operate. Here I offer two variants of such a model. In one variant, juve- nile hosts obtain microbiomes from their parents (lineal inheritance). In the other variant, microbiomes of juvenile hosts are assembled from source pools representing the combined microbiomes of all parents (collective inheritance). According to both variants, holobiont selection causes evolutionary change in holobiont traits and thus is plausibly an important evolutionary force. Holobiont selection as an important evolutionary force is supported by mathematical model. 1 bioRxiv preprint doi: https://doi.org/10.1101/465310; this version posted December 12, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.
    [Show full text]
  • The Holobiont with Its Hologenome Is a Level of Selection in Evolution
    Swarthmore College Works Biology Faculty Works Biology 2018 The Holobiont With Its Hologenome Is A Level Of Selection In Evolution Scott F. Gilbert Swarthmore College, [email protected] E. Rosenberg I. Zilber-Rosenberg Follow this and additional works at: https://works.swarthmore.edu/fac-biology Part of the Biology Commons Let us know how access to these works benefits ouy Recommended Citation Scott F. Gilbert, E. Rosenberg, and I. Zilber-Rosenberg. (2018). "The Holobiont With Its Hologenome Is A Level Of Selection In Evolution". Landscapes Of Collectivity In The Life Sciences. 305-324. https://works.swarthmore.edu/fac-biology/549 This work is brought to you for free by Swarthmore College Libraries' Works. It has been accepted for inclusion in Biology Faculty Works by an authorized administrator of Works. For more information, please contact [email protected]. The Holobiont with Its Hologenome Is·a Level of Selection in 24 Evolution · Scott F. Gilbert, Eugene Rosenberg, and Ilana Zilber-Rosenberg Symbiosis-once thought to be a peripheral phenomenon-is the hallmark oflife on Earth, from genomes through ecosystems (Gordon 2012). What concerns us here is the level of the organism. Symbiosis is replacing an essentialist conception of "individuality" with a new conception, the holobiont, which is a multilineage biological entity, and, we argue, a major level of natural selection. Zoological organisms have traditionally been defined as individuals on the bases of anatomical, embryological, physiological, immunological, genetic, or evolutionary criteria (Geddes and Mitchell 1911; Clarke 2010; Nyhart and Lidgard 2011; see Gilbert et al. 2012). These conceptions, though, are not wholly inde­ pendent of one another, and each of these definitions stems from the common tenet of genomic individuality: an individual contains a single genome.
    [Show full text]