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t is widely accepted that all animals
and plants host diverse microbial com-
munities that are vitally important for
their functioning and survival. In many
cases, these microbiomes can be at least
partially heritable, being passed from
parent to offspring. Thus, when environ-
mental changes occur, we would expect
to see alterations not only in hosts’ physi-
ology over subsequent generations, but
also in their microbiomes.
Husband-and-wife team Eugene
Rosenberg and Ilana Zilber-Rosenberg
of Te l Aviv University in Israel were the
first researchers to propose this con-
cept (FEMS Microbiol Rev, 32:723–35,
2008). A host organism and its resi-
dent microbes—the so-called holobi-
ont—functions as a whole on multiple
levels, they argued, from the gene and
chromosome to the organism’s anatomy
and physiology, and acts as an indepen-
dent unit of selection.
A famous example of this concept
is the relationship between corals and
their symbionts, the zooxanthellae.
Researchers have demonstrated that
some corals can evolve to tolerate
higher water temperatures by chang-
ing the makeup of their symbiont
communities. Because microbes have
much shorter generation times than
coral polyps, the genetic composition
of the symbiont populations can evolve
much more rapidly than that of their
hosts, and these changes can confer
higher tolerance on the holobiont unit.
Over the last decade, it has become
evident that the idea of the evolution-
ary concept of the hologenome, which
views the holobiont as the unit of
selection, can be applied across the
tree of life, with examples cropping up
in plants and insects. This revelation
motivated us to explore the relevance
of the microbiome to the adaptationof so-called poikilothermic animals,
which are unable to maintain a stable
body temperature using internal
mechanisms. Specifically, we set out
to answer whether host selection for
an environmental stressor such as cold
exposure results in selection of fishes’
associated microbes.
We bred tropical blue tilapia,
which are typically found in marine
environments with high water temper-
atures of 24–28 °C. Over three gen-
erations, we selected for fish whose
siblings had high survival rates in low-
temperature conditions. We then com-
pared the gut microbiomes of genet-
ically cold-resistant fish to those of
cold-sensitive fish. Despite having
never experienced low-temperature
environments themselves, these two
groups had different gut microbiomes
as a result of the selection. Moreover,
when we challenged all these fish in
low-temperature conditions, cold-
resistant fish’s gut microbiomes weremore stable, as were the fish’s tran-
scriptomes. Thus, our selection regime
shaped both the host and its associ-
ated microbiome to be more resil-
ient to drops in temperature (eLife,
7:e36398, 2018).
These findings are no doubt just
one example of coordination between
a host and its microbes. As the evo-
lutionary concept of the hologenome
matures, researchers will likely docu-
ment many more plant and animal
communities that evolve with their
microbiomes. It remains to be deter-
mined whether a microbiome’s com-
positional changes directly affect its
host’s physiological response to chang-
ing environmental conditions. But the
holo genome concept will undoubtedly
influence our understanding of the evo-
lution and ecology of all organisms. g
Itzhak Mizrahi is an Associate
Professor at Ben-Gurion University in
Israel. Fotini Kokou is a postdoctoral
fellow in his group.More Than the Sum of Its Parts
The study of evolution requires consideration of organisms’ microbiomes.BY ITZHAK MIZRAHI AND FOTINI KOKOUCRITIC AT LARGE