The Hologenome Concept: Helpful or Hollow?

With the increasing appreciation for the crucial roles that microbial symbionts play in the development and fitness of plant and animal hosts, there has been a recent push to interpret evolution through the lens of the “hologenome”—the collective genomic content of a host and its microbiome. But how symbionts evolve and, particularly, whether they undergo natural selection to benefit hosts are complex issues that are associated with several misconceptions about evolutionary processes in host-associated microbial communities. Microorganisms can have intimate, ancient, and/or mutualistic associations with hosts without having undergone natural selection to benefit hosts. Likewise, observing host-specific microbial community composition or greater community similarity among more closely related hosts does not imply that symbionts have coevolved with hosts, let alone that they have evolved for the benefit of the host. Although selection at the level of the symbiotic community, or hologenome, occurs in some cases, it should not be accepted as the null hypothesis for explaining features of host–symbiont associations.

• Publication year

  2015

• Venue

  PLoS Biology

• Publication date

  2015-12-01

• Fields of study

  Biology, Medicine, Philosophy, Environmental Science

• Identifiers
  DOI 10.1371/journal.pbio.1002311PMID 26636661PMCID 4670207
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Relatedness, Conflict, and the Evolution of Eusociality

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  2015influential reference
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  2014influential reference
• Metamorphosis of a Butterfly-Associated Bacterial Community

  2014cited by this paper
• Superorganisms and Holobionts

  2013cited by this paper
• The gut microbiota of insects - diversity in structure and function.

  2013cited by this paper
• Animals in a bacterial world, a new imperative for the life sciences

  2013influential reference
• Distinct antimicrobial peptide expression determines host species-specific bacterial associations

  2013cited by this paper
• The gut microbiota — masters of host development and physiology

  2013cited by this paper
• The Hologenomic Basis of Speciation: Gut Bacteria Cause Hybrid Lethality in the Genus Nasonia

  2013cited by this paper
• The central role of the host cell in symbiotic nitrogen metabolism

  2012cited by this paper
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  2012cited by this paper
• A bacterial sulfonolipid triggers multicellular development in the closest living relatives of animals

  2012cited by this paper
• Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte–embryo interface

  2012influential reference
• Insect Herbivores Drive Real-Time Ecological and Evolutionary Change in Plant Populations

  2012cited by this paper
• THE ROLES OF HOST EVOLUTIONARY RELATIONSHIPS (GENUS: NASONIA) AND DEVELOPMENT IN STRUCTURING MICROBIAL COMMUNITIES

  2012cited by this paper
• The making of a photosynthetic animal

  2011cited by this paper
• Bacterial Communities of Diverse Drosophila Species: Ecological Context of a Host–Microbe Model System

  2011cited by this paper
• Low-diversity bacterial community in the gut of the fruitfly Drosophila melanogaster.

  2011cited by this paper
• Aphid genome expression reveals host–symbiont cooperation in the production of amino acids

  2011cited by this paper
• Selection patterns on restorer-like genes reveal a conflict between nuclear and mitochondrial genomes throughout angiosperm evolution

  2011cited by this paper
• Evolutionary Relationships of Wild Hominids Recapitulated by Gut Microbial Communities

  2010cited by this paper
• Adaptation via Symbiosis: Recent Spread of a Drosophila Defensive Symbiont

  2010cited by this paper
• The hologenome theory of evolution contains Lamarckian aspects within a Darwinian framework.

  2009cited by this paper
• Opportunistic pathogens enriched in showerhead biofilms

  2009cited by this paper
• Genomics and evolution of heritable bacterial symbionts.

  2008cited by this paper
• Wolbachia: master manipulators of invertebrate biology

  2008cited by this paper
• Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution.

  2008influential reference
• The Bacterial Symbiont Wolbachia Induces Resistance to RNA Viral Infections in Drosophila melanogaster

  2008cited by this paper
• The role of microorganisms in coral health, disease and evolution

  2007cited by this paper
• Colloquium Papers: Symbiosis as an adaptive process and source of phenotypic complexity

  2007cited by this paper
• The winnowing: establishing the squid–vibrio symbiosis

  2004cited by this paper
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  2003cited by this paper
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  2002cited by this paper
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  2002cited by this paper
• Conflicting levels of selection in the accumulation of mitochondrial defects in Saccharomyces cerevisiae

  2002cited by this paper
• Male-killing bacteria in insects: mechanisms, incidence, and implications.

  2000cited by this paper
• Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS

  2000cited by this paper
• Mutual policing and repression of competition in the evolution of cooperative groups

  1995cited by this paper
• Phylogenetic consequences of symbioses: Eukarya and Eubacteria are not monophyletic taxa.

  1992cited by this paper
• 历史生物地新趋势—分衍生物地理学（Vicariance Biogeography）

  1990influential reference
• Evolution of Specialization in Insect-Umbellifer Associations

  1990cited by this paper
• Evolution of Insect/Host Plant Relationships

  1984cited by this paper
• Adaptation and Natural Selection: A Critique of Some Current Evolutionary Thought. George C. Williams

  1969cited by this paper
• BUTTERFLIES AND PLANTS: A STUDY IN COEVOLUTION

  1964cited by this paper
• Animal Dispersion in Relation to Social Behaviour.

  1963cited by this paper
• Animal dispersion in relation to social behaviour

  1962cited by this paper

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