Discussion
Using detailed multihost, multiparasite time series data and network
analysis approaches, we estimated potential cross-species transmission
in Daphnia communities. We found evidence that parasites in these
lakes differ in their ability to infect and transmit between host
species; three parasites showed high host breadth and strong potential
for cross-species transmission (based on high overlap of epidemics in
different host species in a given lake on a given date). Focusing on
these three common multihost parasites, two hosts, D. retrocurvaand the well-studied D. dentifera , are most implicated in
cross-species transmission. This was particularly true for the bacteriumP. ramosa . In contrast, for another common multihost parasite,
the bacterium S. cienkowskii , cross-species transmission seemed
less reliant on particular species.
Basing our estimates of plausible cross-species transmission on
synchrony of single pathogen epidemics, we found that the identity of
both the pathogen and host species were important to our networks.
Pathogens varied in their specificity of host species and in their
apparent ability to transmit among host species. With one notable
exception, pathogen species with greater host breadth (implying lesser
specificity) displayed greater potential for cross-species transmission.
The exception is G. vavrai; this parasite was found to infect
multiple host species, but epidemics were separated in time leaving no
potential for cross-species transmission. Notably, it has been suggested
that an intermediate, non-Daphnia host, is required for theG. vavrai lifecycle (Refardt et al. 2002), which would preclude
cross-species transmission among Daphnia in our communities for
this pathogen. This is also the case for the other pathogen for which we
found no potential cross-species transmission, L. obtusa (Refardt
et al. 2002). These results thus provide support for our method of cross
species transmission detection.
For our three most common pathogens, our estimates of network centrality
indicate that host identity plays a strong role in potential for cross
species transmission, with some host species having a disproportionate
influence on community transmission. However, the degree to which host
identity influenced cross species transmission – and the particular
host(s) that most strongly impacted it – varied by pathogen. For two of
our pathogens, a subgroup of hosts were more central within the network
(supporting greater cross species transmission), while for the third,S. cienkowskii, no host displayed greater cross species
transmission potential. Thus, this approach allows us to identify
pathogen species for which some hosts might have an outsized impact on
disease dynamics in these communities, and also gives us insight into
multihost-multiparasite communities as a whole. The potential patterns
of interspecific transmission for P. ramosa can be more readily
studied in lab experiments, as compared to those for S.
cienkowskii ; while experimental infections with S. cienkowskiiare possible, they are rare and experiments are challenging. Thus,
instead, molecular analyses of infections in these species seem more
promising. A study of P. ramosa in these lake populations
genotyped the parasite primarily from D. retrocurva and D.
dentifera (based on the availability of infected hosts in the field),
but also included several infected D. parvula and oneCeriodaphnia dubia (Shaw 2019; Shaw et al. in review). In this
analysis, the genotypes found in D. parvula were always also
found in D. retrocurva , but the same genotype was not found
infecting both D. dentifera and D. retrocurva . Thus, the
molecular results partially support the analyses here that indicate thatP. ramosa moves between host species, but also suggests there are
barriers to doing so that are not captured by these analyses. Molecular
analyses of S. cienkowskii -infected hosts from natural
populations would be interesting; based on the network analyses, we
predict less genetic structuring by host species for S.
cienkowskii .
Parasites differ in their ability to infect and transmit among different
host species, though we cannot yet say why some parasite species
commonly infect more host species in the same site; both pathogen life
history traits and taxonomic group have been suggested as potential
mechanisms (Pedersen et al. 2005). Our two bacterial parasites, S.
cienkowskii and P. ramosa , generally had higher host breadth and
potential cross-species transmission compared to other parasites;
however, the oomycete parasites, B. paedophthorum and ‘Spider’,
significantly differed in both host breadth and potential cross species
transmission. Moreover, more recent work on a microsporidian gut
parasite that was not included in this study, O. pajunii , has
found substantial transmission across host species (Dziuba et al. 2023).
Overall, these results make it difficult to conclude whether taxonomic
group strongly influences the likelihood of cross species transmission.
We know that these parasites differ in key aspects of their
transmission, with some (e.g., B. paedophthorum ) being
continually shed and others (e.g., P. ramosa, S. cienkowskii , andM. bicuspidata ) being obligate killers. Moreover, within a
parasite species, particular aspects of phenotype or genotype can
influence transmission. In P. ramosa , only certain genotypes can
attach to the esophagus of the host, a key first step in infection
(Duneau et al. 2011; Ebert et al. 2015); when this occurs across
species, infections often fail at a later (but currently unknown) stage
in the infection process (Luijckx et al. 2014). In contrast, withM. bicuspidata , interspecific transmission seems to be asymmetric
and to depend on parasite genotype and spore size (Shaw et al. 2021; Sun
et al. 2023). Future studies that aim to uncover the traits that promote
– or prevent – cross species transmission will help us better
understand and predict infections in complex natural communities.
Host species differed in the pathogens they hosted and in their relative
potential importance for cross species transmission (Fig 4). Phylogeny
can influence patterns of cross-species transmission (Streicker et al.
2010; Parker et al. 2015; Mollentze and Streicker 2020). In particular,
hosts might be more susceptible to parasites transmitted from more
closely related host species. Our P. ramosa network suggests thatCeriodaphnia are significantly less likely to be involved in
cross species transmission than Daphnia species, supporting a
phylogenetic influence for this pathogen. This is consistent with the
limited experimental evidence we have, which suggests that cross species
transmission between C. dubia and D. dentifera is
possible, but rare (Auld et al. 2017). It is also consistent with
genetic evidence collected in 2015 (overlapping with this study), which
found that the P. ramosa strain in C. dubia was an
outgroup to the strains in Daphnia (Shaw 2019; Shaw et al. in
review)). In contrast, our results for B. paedophthorum do not
suggest challenges traversing greater phylogenetic distances, asC. dubia did not differ from the Daphnia hosts displaying
the greatest transmission potential. This is also consistent with
experimental studies, which were readily able to transmit this parasite
across host species (Duffy et al. 2015). As P. ramosa is known to
have a matching allele interaction with hosts (Bento et al. 2017), it is
probable that pathogens with this infection strategy are more likely to
have phylogenetically regulated cross-species transmission.
Within our communities, we saw variation in epidemic size within our
pathogens. Focusing on the three pathogens for which we were able to
create networks, we found that two (P. ramosa and B.
paedophthorum ) displayed significant differences in infected host
density among host species (Fig 5). The patterns in infected host
density closely replicated the patterns for centrality among hosts (Fig
4, Fig 5). Our remaining pathogen, S. cienkowski , displayed no
differences in epidemic size by host and also no differences in host
centrality among hosts. Previous work has demonstrated a positive
(though nonlinear) causal relationship of infected host density to
within species transmission (Rachowicz and Briggs 2007; Roberts and
Hughes 2015). As centrality, here, represents potential cross-species
transmission, our results suggest that infected host density (or
epidemic size) within host species may also influence cross-species
transmission. Thus, these results extend known within species
transmission mechanisms to the multi host species scale.
We are beginning to disentangle the ecological and epidemiological
drivers of cross species transmission (Lloyd-Smith et al. 2009;
Plowright et al. 2015; Plowright et al. 2017). However, we still lack
the ability to accurately predict novel transmission events and host
shifts, or the degree to which cross species transmission maintains
epidemics within communities (Mollentze and Streicker 2020). By applying
network analysis techniques to a rich dataset from a well-studied
planktonic host-parasite system, we were able to uncover host species
that seem particularly important for maintaining levels of infection in
a community, as well as differences among parasite species in the degree
to which they infect multiple host species. Because of its correlative
nature, this work cannot definitively say whether certain host or
parasite species are more involved in cross-species transmission, but it
can inform hypotheses about transmission patterns within this community.
For example, it suggests that parasites differ in the degree to which
host phylogeny constrains their ability to spillover between hosts
(e.g., P. ramosa vs. S. cienkowskii ). In doing so, it
points to additional studies that will help us better understand this
system (e.g., studies characterizing the genetic diversity of P.
ramosa vs. S. cienkowskii in different host species during
epidemic outbreaks). More broadly, it provides additional support for
the value of network approaches for providing insights into patterns of
transmission in nature and for generating hypotheses regarding
transmission in complex multihost-multiparasite communities.