Hologenome theory

Hologenome Theory Definition

The framework of the hologenome theory of evolution is as follows (condensed from Rosenberg et al., 2007):²²

"All animals and plants establish symbiotic relationships with microorganisms."

"Different host species contain different symbiont populations and individuals of the same species can also contain different symbiont populations."

"The association between a host organism and its microbial community affect both the host and its microbiota."

"The genetic information encoded by microorganisms can change under environmental demands more rapidly, and by more processes, than the genetic information encoded by the host organism."

"... the genome of the host can act in consortium with the genomes of the associated symbiotic microorganisms to create a hologenome. This hologenome...can change more rapidly than the host genome alone, thereby conferring greater adaptive potential to the combined holobiont evolution."

"Each of these points taken together Rosenberg et al. to propose that the holobiont with its hologenome should be considered as the unit of natural selection in evolution."

Some authors supplement the above principles with an additional one. If a given holobiont is to be considered a unit of natural selection:

The hologenome must be heritable from generation to generation.²⁴" target="_blank" rel="noopener">Ten principles of holobionts and hologenomes were presented in PLOS Biology^[3 to clarify and append what these terms and concepts are and are not, to explain how they both support and extend existing theory in the life sciences, and to discuss their potential ramifications for the multifaceted approaches of zoology and botany

I. Holobionts and hologenomes are units of biological organization

II. Holobionts and hologenomes are not organ systems, superorganisms, or metagenomes

III. The hologenome is a comprehensive gene system

IV. The hologenome concept reboots elements of Lamarckian evolution

V. Hologenomic variation integrates all mechanisms of mutation

VI. Hologenomic evolution is most easily understood by equating a gene in the nuclear genome to a microbe in the microbiome

VII. The hologenome concept fits squarely into genetics and accommodates multilevel selection theory

VIII. The hologenome is shaped by selection and neutrality

IX. Hologenomic speciation blends genetics and symbiosis

X. Holobionts and their hologenomes do not change the rules of evolutionary biology
 

Horizontally versus vertically transmitted symbionts

Many case studies clearly demonstrate the importance of an organism's associated microbiota to its existence. (For example, see the numerous case studies in the Microbiome article.) However, horizontal versus vertical transmission of endosymbionts must be distinguished. Endosymbionts whose transmission is predominantly vertical may be considered as contributing to the heritable genetic variation present in a host species.^{In the case of colonial organisms such as corals, the microbial associations of the colony persist even though individual members of the colony, reproducing asexually, live and die. Corals also have sexual mode of reproduction, resulting in planktonic larva; it is less clear whether microbial associations persist through this stage of growth. Also, the bacterial community of a colony may change with the seasons.[17}

Many insects maintain heritable obligate symbiosis relationships with bacterial partners. For example, normal development of female wasps of the species Asobara tabida is dependent on Wolbachia infection. If "cured" of the infection, their ovaries degenerate.²⁵ Transmission of the infection is vertical through the egg cytoplasm.

In contrast, many obligate symbiosis relationships have been described in the literature where transmission of the symbionts is via horizontal transfer. A well-studied example is the nocturnally feeding squid Euprymna scolopes, which camouflages its outline against the moonlit ocean surface by emitting light from its underside with the aid of the symbiotic bacterium Vibrio fischeri.^{Rosenbergs cite this example within the context of the hologenome theory of evolution.[27} Squid and bacterium maintain a highly co-evolved relationship. The newly hatched squid collects its bacteria from the sea water, and lateral transfer of symbionts between hosts permits faster transfer of beneficial mutations within a host species than are possible with mutations within the host genome.

Primary versus secondary symbionts

Green Vegetable Bug (Nezara viridula) inFronton, France

Another traditional distinction between endosymbionts has been between primary and secondary symbionts.^{endosymbionts reside in specialized host cells that may be organized into larger, organ-like structures (in insects, thebacteriome). Associations between hosts and primary endosymbionts are usually ancient, with an estimated age of tens to hundreds of millions of years. According to endosymbiotic theory, extreme cases of primary endosymbionts includemitochondria, plastids (including chloroplasts), and possibly other organelles of eukaryotic cells. Primary endosymbionts are usually transmitted exclusively vertically, and the relationship is always mutualistic and generally obligate for both partners. Primary endosymbiosis is surprisingly common. An estimated 15% of insect species, for example, harbor this type of endosymbiont.[28} In contrast, secondary endosymbiosis is often facultative, at least from the host point of view, and the associations are less ancient. Secondary endosymbionts do not reside in specialized host tissues, but may dwell in the body cavity dispersed in fat, muscle, or nervous tissue, or may grow within the gut. Transmission may be via vertical, horizontal, or both vertical and horizontal transfer. The relationship between host and secondary endosymbiont is not necessarily beneficial to the host; indeed, the relationship may be parasitic.^{The distinction between vertical and horizontal transfer, and between primary and secondary endosymbiosis is not absolute, but follows a continuum, and may be subject to environmental influences. For example, in the stink bug Nezara viridula, the vertical transmission rate of symbionts, which females provide to offspring by smearing the eggs with gastric caeca, was 100% at 20 °C, but decreased to 8% at 30 °C.[29}Likewise, in aphids, the vertical transmission of bacteriocytes containing the primary endosymbiont Buchnera is drastically reduced at high temperature.³⁰ In like manner, the distinction between commensal, mutualistic, and parasitic relationships is also not absolute. An example is the relationship between legumes and rhizobial species: N₂ uptake is energetically more costly than the uptake of fixed nitrogen from the soil, so soil N is preferred if not limiting. During the early stages of nodule formation, the plant-rhizobial relationship actually resembles a pathogenesis more than it does a mutualistic association.
 

Hologenome in Neo-Lamarckism within a Darwinian context

Lamarckism, the concept that an organism can pass on characteristics that it acquired during its lifetime to its offspring (also known as inheritance of acquired characteristics or soft inheritance) incorporated two common ideas of its time:

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Use and disuse – individuals lose characteristics they do not require (or use) and develop characteristics that are useful.

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Inheritance of acquired traits – individuals inherit the traits of their ancestors.

Although Lamarckian theory was rejected by the neo-Darwinism of the modern evolutionary synthesis in which evolution occurs through random variations being subject to natural selection, the hologenome theory has aspects that harken back to Lamarckian concepts. In addition to the traditionally recognized modes of variation (i.e. sexual recombination, chromosomal rearrangement, mutation), the holobiont allows for two additional mechanisms of variation that are specific to the hologenome theory: (1) changes in the relative population of existing microorganisms (i.e.amplification and reduction) and (2) acquisition of novel strains from the environment, which may be passed on to offspring.²⁷

Changes in the relative population of existing microorganisms corresponds to Lamarckian "use and disuse", while the ability to acquire novel strains from the environment, which may be passed on to offspring, corresponds to Lamarckian "inheritance of acquired traits". The hologenome theory, therefore, is said by its proponents to incorporate Lamarckian aspects within a Darwinian framework.