R. insecticola greatly reduces fitness costs associated
with APV infection, but H. defensa exacerbates costs
Persistent infection by APV was previously reported to reduce pea aphid
fitness (Van den Heuvel et al. 1997, Lu et al. 2020). However, these
studies did not control for aphid genotype or the presence of
facultative symbionts, which occur in most pea aphids and are known to
confer protection to specialized natural enemies (Russell et al. 2013,
Oliver et al. 2014). Here, we generalize prior findings by showing that
persistent APV infections reduced aphid fecundity and survival across
multiple pea aphid genotypes lacking facultative symbionts (Table 3). In
aphids without facultative symbionts, we also found that APV titer
exhibited similar trajectories over aphid lifespan, which is consistent
with the infection costs we observed (Fig. 4).
When we examined our experimental lines with and without two common and
closely related protective facultative symbionts H. defensa andR. insecticola, we found that the fitness of aphids with
persistent APV infections varied dramatically depending on which
symbiont was present. In aphids carrying R. insecticola , costs to
persistent infection with APV were largely eliminated (Fig 2A-B, Table
3). Not only were fitness estimates similar between R.
insecticola carrying aphids with and without APV, but aphids with both
APV and R. insecticola produced statistically similar numbers of
offspring compared to the control line (no APV or symbiont). APV
abundance was also lower in aphids with R. insecticola versus
those without this symbiont, although significantly so only in older
aphids (Fig. 4A). Taken together, these results indicate that R.
insecticola provides substantial protection against infection with APV.
To our knowledge, R. insecticola represents only the second
heritable symbiont known to confer protection against viral pathogens.
Some strains of the ubiquitous Wolbachia symbiont confer
protection against specialized RNA viruses in natural hosts (Hedges et
al. 2008, Teixeira et al. 2008, Pimentel et al. 2021). ThoughWolbachia’s pathogen blocking mechanisms remain poorly
understood, and may vary between natural and novel associations,
hypotheses include immune priming, resource competition, or modification
of the host cell environment (Terradas and McGraw 2017, Lindsey et al.
2018). Associations between anti-viral Wolbachia strains
introduced into important insect vectors are actively being researched
and applied in real-world efforts to mitigate human disease such as
dengue (Nazni et al. 2019, O’Neill et al. 2019). Hence, having a second
heritable symbiont with anti-viral properties in a system with
unparalleled in vivo experimental protocols and developingin vitro ones (Brandt et al. 2017, Patel et al. 2019) provides
excellent opportunities to develop an additional model of anti-viral
symbiosis. One caveat to our study is that we only examined a single
strain of R. insecticola in one aphid background. However, this
is by far the most common of only two strains recovered from recent
surveys of N. American pea aphids on alfalfa (Peng et al. 2022). And
given prior findings that R. insecticola improves pea aphid
fitness in the presence of specialized fungal pathogens (Parker et al.
2013), and when coinfecting aphids alongside costly strains of the
facultative symbionts H. defensa and Spiroplasma(Mathé-Hubert et al. 2019, Weldon et al. 2020), this appears to be a
common phenotype associated with R. insecticola .
In contrast to R. insecticola , APV infection costs were
significantly exacerbated in aphid lines carrying H. defensa(Table 3C & D) and H. defensa did not influence APV abundance
(Fig. 2D-I & Fig. 4). While symbionts that protect hosts receive the
most interest, those that enhance pathogen infection are nonetheless
important for natural symbiont maintenance and disease dynamics (Graham
et al. 2012, Amuzu et al. 2018).