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\begin{document}

\title{PREreview of bioRxiv article ``A generalist pathogen view of diverse
host evolutionary histories through polygenic virulence''}



\author[1]{Sophien Kamoun}%
\affil[1]{The Sainsbury Laboratory}%


\vspace{-1em}



  
  \date{May 26, 2024}


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\begin{abstract}
This is a review of Caseys et al. bioRxiv doi:
\url{https://doi.org/10.1101/507491} posted on June 25, 2019. This study
aims at addressing whether coevolutionary models of host-pathogen
interactions apply to a generalist pathogen that exhibits quantitative
virulence across a broad range of plants. They generated an exhaustive
virulence matrix for the nectrophic fungus \emph{Botrytis cinerea} on 90
genotypes of 8 plant species. They conclude that this pathosystem
doesn't fit traditional arms-race coevolution models with quantitative
variation in susceptibility distinct from the phylogenetic relationships
between the examined plants.%
\end{abstract}%



\sloppy


\section*{Main Comments}

{\label{143940}}

This study aims at addressing the important question of whether
coevolutionary models of host-pathogen interactions apply to a
generalist pathogen that exhibits quantitative virulence across a broad
range of plants. They generated an exhaustive virulence matrix for the
nectrophic fungus \emph{Botrytis cinerea} on 90 genotypes of 8 plant
species. They conclude that this pathosystem doesn't fit traditional
arms-race coevolution models with quantitative variation in
susceptibility distinct from the phylogenetic relationships between the
examined plants.

The paper reports interesting data and is framed around an evolutionary
message. They draw strong conclusions about how the \emph{Botrytis}
pathosytem drastically differs from classic arms-race evolutionary
models of plant-pathogen interactions. Although, I wouldn't be surprised
that this fascinating and still poorly understood generalist fungus
would display unique features, I'm not convinced that the evolutionary
conclusions are justified based on the described experiments.~

One issue is sampling. The majority of the isolates are from grapes, yet
grapes are not tested as a host and the assays involve a mix of plant
species and genotypes that may have never been exposed to the California
grape population of the fungus. This is a serious experimental issue as
the paper centers on coevolutionary arguments yet the dominant
coevolutionary system in the sample collection (\emph{B. cinerea} vs
grape) is never tested.

A related point is that coevolutionary models of host-pathogen
interactions imply coevolution at the level of local host/pathogen
populations whereas the sampled fungus strains and host plants tested
here are not supported by an ecological/biological rationale. In fact,
besides the California grape isolates, the pathogen samples are from a
global population and there is no evidence as far as I know that for
example Arabidopsis is naturally infected by~\emph{B. cinerea}. Thus I
do question whether evolutionary statements can be drawn from the
studied pathogen/host collection in the absence of ecological or
biological evidence of coevolution.

In addition, the inclusion of crop species is an issue as far as
generating coevolutionary hypotheses. Does variation in genetic
resistance in these crops reflect coevolutionary dynamics or is it an
indirect consequence of crop domestication and breeding for other
traits.

I'm also concerned about drawing general conclusions about strain host
specificity as the coefficient of variation of mean lesion area across
the plant species. First, this is~based on single measurements and
doesn't take into account other aspects of the infection cycle which may
be more relevant to the coevolutionary dynamics. Second, averaging can
be misleading given that specialization by definition means decreased
virulence on alternative hosts. Thus the statement ``strains with
increased host specificity had on average lower virulence across all
Eudicots'' is neither surprising nor contradictory to theoretical
expectations as stated. This is exactly what one would expect for
~typical specialist strains.

Another issue is the impact of these interactions on pathogen and plant
fitness, which are important to appreciate before drawing evolutionary
models. Although~\emph{B. cinerea~}can indeed be a destructive pathogen
in agricultural systems it is unclear to this reviewer how it impacts
the fitness of its native host plants; and vice versa the extent to
which this pathogen relies on plant infection for its reproduction
(unlike say an obligate biotroph). To me this is a critical part of the
comparison between~\emph{B. cinerea~}and other pathogens/parasites that
have unequivocal negative impact on their hosts and/or are dependent on
their hosts leading to strong selection dynamics for
resistance/virulence. In other words, strong selection pressures are an
important aspect of the equation when weighing theoretical expectations
for an arms race.

It is also important to point out that there are notable examples of
pathogens that exhibit clear arms race dynamics and quantitative
variation in virulence, but somehow infect phylogenetically unrelated
plant species. These include~\emph{Phytophthora capsici~}(pepper and
cucurbits),~\emph{Phytophthora palmivora~}(monocots and dicots), the
multihost rust fungi and others. Even though these pathogens infect a
phylogenetically discontinuous range of host plants, individual
genotypes of their host species can exhibit classic strong genetic
resistance. This context is important for the discussing the observation
that variation in plant susceptibility does not track plant phylogeny.

\section*{Other comments}

{\label{269240}}

Figure 3 clearly shows that \emph{C. endivia} has a distinct pattern of
susceptibility compared to the other taxa. In fact, there is even a
cluster of \emph{B. cinerea} strains that seem more aggressive on
\emph{C. endivia} than on any of the other plants tested. Not sure how
these observation fit with the conclusion about absence of connections
between susceptibility vs plant phylogeny and the lack of
specialization.

\section*{Reviewers}

{\label{926656}}

Sophien Kamoun. The Sainsbury Laboratory, Norwich Research Park,
University of East Anglia, Norwich, UK.

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