Getting the Hologenome Concept Right: An Eco-Evolutionary Framework for Hosts and Their Microbiomes

Abstract

Given the complexity of host-microbiota symbioses, scientists and philosophers are asking questions at new biological levels of hierarchical organizationwhat is a holobiont and hologenome? When should this vocabulary be applied? Are these concepts a null hypothesis for host-microbe systems or limited to a certain spectrum of symbiotic interactions such as host-microbial coevolution? Critical discourse is necessary in this nascent area, but productive discourse requires that skeptics and proponents use the same lexicon. For instance, critiquing the hologenome concept is not synonymous with critiquing coevolution, and arguing that an entity is not a primary unit of selection dismisses the fact that the hologenome concept has always embraced multilevel selection. Holobionts and hologenomes are incontrovertible, multipartite entities that result from ecological, evolutionary, and genetic processes at various levels. They are not restricted to one special process but constitute a wider vocabulary and framework for host biology in light of the microbiome.

Phylosymbiosis: Relationships and Functional Effects of Microbial Communities across Host Evolutionary History

“…It is worth emphasizing again that this term is explicit and different from many other similar terms, such as coevolution, cospeciation, cocladogenesis, or codiversification [73]. While cospeciation of hosts and specific environmentally or socially acquired microbes—e.g., hominids and gut bacterial species [74] or the bobtail squid and Vibrio luminescent bacteria [75]—could contribute in part to phylosymbiosis, concordant community structuring with the host phylogeny is not dependent on parallel gene phylogenies but instead on total microbiota compositional divergence.…”

Holobionts and the ecology of organisms: Multi-species communities or integrated individuals?

“…The term first found wide usage in coral biology where it was defined as a coral colony and its associated photosynthetic algal symbionts and bacterial communities (Rohwer et al 2002, Knowlton and Rohwer 2003, Stat et al 2012. The recent influx of interest in macrobe-microbe relations has led to a proliferation of the term "holobiont", now most often understood as a host macroorganism and all of its associated microbiota, including bacteria, archaea, viruses, protists, fungi, and microscopic multicellular animals such as nematodes (Zilber-Rosenberg and Rosenberg 2008, Booth 2014, Bordenstein and Theis 2015, Moran and Sloan 2015, Douglas and Werren 2016, Theis et al 2016. Because the holobiont includes all associated microbiota, the interactions between holobiont partners may be harmful, beneficial or of no consequence.…”

Rapid adaptive responses to climate change in corals

“…Rapid responses in the coral-associated microbiome do not need to rely on mutation, but may arise from changes in the relative abundance (or lifestyles, for example, pathogenic switch) of associated microorganisms, acquisition of novel microbes (with novel functions) from the environment, or horizontal gene transfer among microbes 106 . Importantly, most of these processes have not been tested or unequivocally proven in the coral holobiont system, highlighting an important research priority 87 .…”