Discussion
It has been shown that hosts receive the greatest benefits from
protective microbes under constant pathogen infection. We hypothesized
that variation in pathogen presence over time would limit the evolution
of microbe-mediated protection due to the reduced benefits to the host
and bacterial symbiont. In our study, enhanced pathogen defence emerged
out of host-symbiont coevolutionary interactions only when pathogens
were present, independent of the interval or initial presence of the
pathogen. Notably, the ultimate strength of microbe-mediated protection
that evolved was not impacted by the number of host generations between
pathogen infections, the proportion of generations infected, or the
presence of the pathogen at the first host-microbe interaction. These
results suggest that resident microbes can be a form of
transgenerational immunity against rare pathogen infections.
We found that microbe-mediated protection is maintained even in the
prolonged absence of pathogen, but that pathogen presence is necessary
for microbe-mediated protection to evolve, as previously hypothesized
(Clay et al., 2005; King and Bonsall, 2017; Lively et al., 2005). This
result is unlike previous work showing that the scale of heterogeneity
in abiotic conditions can affect the strength of selection for traits in
some symbiotic interactions (Harrison et al., 2013). This discrepancy is
potentially due to costs in our symbiotic system being ameliorated (at
least in terms of host survival) in well-provisioned hosts, as hosts are
provided with food alongside E. faecalis and are thus rescued
from starvation (also see (Dasgupta et al., 2019)). Although protective
symbionts can incur costs (e.g., Vorburger & Gouskov, 2011) for their
hosts, with potential for impacts on coevolutionary interactions (King
and Bonsall, 2017), it is possible that potential costs of bacterial
colonisation might be only detectable when hosts are stressed (Lively,
2006) or that the costs were not strong enough for us to detect(Little
et al., 2002). Different measures of cost remain to be explored (e.g.
lifespan in the complete absence of a protective microbe and a
pathogen). Higher protection also does not always come with higher
costs, as found in the black bean aphid-Hamiltonella defensainteraction (Cayetano et al., 2015). Thus, protective traits in an
organism’s commensal microbiota could be selected for under pathogen
infection and easily maintained in subsequent uninfected generations.
Microbe-mediated protection was strongest between sympatric pairs when
pathogens were present over evolutionary time, consistent with previous
findings (Rafaluk-Mohr et al., 2018). In our study, protection emerged
during coevolution after only 20 host generations, and not due to the
independent evolution of either interacting species, but due to the
coevolution of both species (King and Bonsall, 2017). The time-scale of
these interactions is short compared to the longer shared evolutionary
histories shared by other defensive mutualisms (Jousselin et al., 2003;
Quek et al., 2004; Shoemaker et al., 2002). Nevertheless, our findings
reveal the potential for microbe-mediated protection to become enhanced
during the formation of a coevolving host-microbiota relationship.
In conclusion, our results show that enhanced protection in host-microbe
interactions can rapidly evolve and be maintained even under infrequent
pathogen infection, suggesting that resident microbes can be a form of
stable, transgenerational immunity. The protective benefit of an
organism’s microbiota might remain undetected for several host
generations until pathogens re-emerge. Future research on the failure of
pathogens transmit within host populations should consider the
contribution of the protective microbiota to prevent disease spread.