The hologenome concept of evolution after 10 years

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. As Darwin wrote, “It is not the strongest of the species that survives but the most adaptable”.

Diet, Gut Microbes and Host Mate Choice

“…[7,11,13,14,15,73] Nevertheless, the discussion of gut microbiomes in Drosophila in the light of this original experiment has been used as support for a role of bacteria in RI. [21] This is a surprising interpretation because the gut microbes of D. melanogaster are reported in these studies to be relatively flexible and acquired from the diet. [74,75] Hence, the composition of the gut community appears to depend upon the specific diet ingested at any particular moment, which varies across an individual's lifetime [76] and may also be different for each sex.…”

“…Nevertheless, the discussion of gut microbiomes in Drosophila in the light of this original experiment has been used as support for a role of bacteria in RI . This is a surprising interpretation because the gut microbes of D. melanogaster are reported in these studies to be relatively flexible and acquired from the diet .…”

“…There is much discussion of whether diet‐associated mating patterns initiated by microbes could represent a new context for kick‐starting RI . In addition, this evidence, together with other observations that gut microbes are causal in determining fitness costs in hybrids (e.g., in Nasonia jewel wasps), is being employed as strong support for the existence of holobionts (the host plus all its symbiotic microbes) as evolutionary units of selection . Proponents of this view argue that host and microbiota should be considered together as a collective whose fitness goals are aligned …”

“…[8,10] In addition, this evidence, together with other observations that gut microbes are causal in determining fitness costs in hybrids (e.g., in Nasonia jewel wasps [16] ), is being employed as strong support for the existence of holobionts (the host plus all its symbiotic microbes) [17] as evolutionary units of selection. [18][19][20][21] Proponents of this view argue that host and microbiota should be considered together as a collective whose fitness goals are aligned. [22] In this article, we discuss the evidence for selection at the level of the holobiont.…”

What viruses tell us about evolution and immunity: beyond Darwin?

“…The horizontal line symbolizes HGT events among the three arms. HGT has been a frequent phenomenon during evolution and is often mediated by viruses and other selfish genetic elements . For example, the human genome contains up to two‐thirds of sequences originating from retroviruses and transposable elements, and at least 145 genes (of a total of 21,000) are likely derived from bacteria, archaea, fungi, protists, and plants .…”