call a “holobiont” (from the Greek, holos, all; biont, life). To summarize, HCE states
that the holobiont is a unit of selection in evolution, such that its hologenome (sum of
the genetic material from the animal/plant plus the genetic material of the members
of the microbiome) is transmitted from one generation to the next pending no
changes in the environment (Suárez Díaz 2019). Thus, the holobiont with its
hologenome is the unit of natural selection upon which evolution works, and
microbial symbionts have a critical role in the adaptation and evolution of higher
organisms. In short, microorganisms are essential not only for the health and
maintenance of individual higher organisms, but they are also a significant factor
in species survival and genetic variation (Rosenberg et al. 2007). Thus, the holobiont
(Margulis 1993; Rohwer et al. 2002) (the host and its symbiotic microbiota) along
with its hologenome, acting together, should be considered a unit of selection in
evolution. The result is that relatively rapid variation in diverse microbial symbionts
plays an important role in the adaptation and evolution of the holobiont (ZilberRosenberg and Rosenberg 2008).
Considerable support exists for the hypothesis that holobionts and their
hologenomes should be considered levels of selection in evolution (Rosenberg and
Zilber-Rosenberg 2018), see also (Suárez Díaz 2019). First, all animals and plants
harbor a diverse microbiota, which is supported by abundant data. The second
principle is that the holobiont functions as a distinct biological entity, and that
interactions between microbiomes and their hosts affect the fitness of their
holobionts. However, the extent to which the microbiota contributes to holobiont
fitness and survival varies enormously. The third principle, whereby the genomes of
both hosts and a significant fraction of their microbiomes are transferred between
generations, is the most contentious but evidence exists in the presence of microbes
in plant seeds (Nelson 2018) and microbial transmission from mother to child in
vaginal birth. The fourth principle, genetic variation in holobionts, occurs when new
symbiotic microorganisms are incorporated in the microbiota. Because microorganisms respond more rapidly and can use multiple mechanisms (including horizontal
gene transfer) to respond to changing environmental conditions, a completely entire
new set of possibilities exists for holobionts to adapt to dramatic environmental
shifts, which are not limited to genetic changes in the host’s genome. ZilberRosenberg and Rosenberg acknowledge that HCE requires not only the existence
of interactions between the host and the symbionts, but that these interactions: (1) are
reliably transmitted transgenerationally and (2) affect the fitness of the holobiont. If
there are host-symbiont interactions that do not exhibit any (or only one) of these two
properties, then the holobiont cannot be considered a unit of selection, but a
conglomerate of independent units of selection interacting ecologically with each
other (Suárez Díaz 2019). In their original paper, Zilber-Rosenberg and Rosenberg
(2008) presented evidence to support the claim that the symbionts that comprise a
holobiont are intergenerationally transmitted with sufficient fidelity to support the
claim that holobionts are units of selection. In their words: “The hologenome theory
of evolution relies on ensuring the continuity of partnerships between holobiont
generations.”
434
S. Kouas et al.
that the holobiont is a unit of selection in evolution, such that its hologenome (sum of
the genetic material from the animal/plant plus the genetic material of the members
of the microbiome) is transmitted from one generation to the next pending no
changes in the environment (Suárez Díaz 2019). Thus, the holobiont with its
hologenome is the unit of natural selection upon which evolution works, and
microbial symbionts have a critical role in the adaptation and evolution of higher
organisms. In short, microorganisms are essential not only for the health and
maintenance of individual higher organisms, but they are also a significant factor
in species survival and genetic variation (Rosenberg et al. 2007). Thus, the holobiont
(Margulis 1993; Rohwer et al. 2002) (the host and its symbiotic microbiota) along
with its hologenome, acting together, should be considered a unit of selection in
evolution. The result is that relatively rapid variation in diverse microbial symbionts
plays an important role in the adaptation and evolution of the holobiont (ZilberRosenberg and Rosenberg 2008).
Considerable support exists for the hypothesis that holobionts and their
hologenomes should be considered levels of selection in evolution (Rosenberg and
Zilber-Rosenberg 2018), see also (Suárez Díaz 2019). First, all animals and plants
harbor a diverse microbiota, which is supported by abundant data. The second
principle is that the holobiont functions as a distinct biological entity, and that
interactions between microbiomes and their hosts affect the fitness of their
holobionts. However, the extent to which the microbiota contributes to holobiont
fitness and survival varies enormously. The third principle, whereby the genomes of
both hosts and a significant fraction of their microbiomes are transferred between
generations, is the most contentious but evidence exists in the presence of microbes
in plant seeds (Nelson 2018) and microbial transmission from mother to child in
vaginal birth. The fourth principle, genetic variation in holobionts, occurs when new
symbiotic microorganisms are incorporated in the microbiota. Because microorganisms respond more rapidly and can use multiple mechanisms (including horizontal
gene transfer) to respond to changing environmental conditions, a completely entire
new set of possibilities exists for holobionts to adapt to dramatic environmental
shifts, which are not limited to genetic changes in the host’s genome. ZilberRosenberg and Rosenberg acknowledge that HCE requires not only the existence
of interactions between the host and the symbionts, but that these interactions: (1) are
reliably transmitted transgenerationally and (2) affect the fitness of the holobiont. If
there are host-symbiont interactions that do not exhibit any (or only one) of these two
properties, then the holobiont cannot be considered a unit of selection, but a
conglomerate of independent units of selection interacting ecologically with each
other (Suárez Díaz 2019). In their original paper, Zilber-Rosenberg and Rosenberg
(2008) presented evidence to support the claim that the symbionts that comprise a
holobiont are intergenerationally transmitted with sufficient fidelity to support the
claim that holobionts are units of selection. In their words: “The hologenome theory
of evolution relies on ensuring the continuity of partnerships between holobiont
generations.”
434
S. Kouas et al.