Discussion
Our results demonstrated that the host specialized aphid can rapidly
adapt to new host plant under assistance of phytopathogen. This is a new
pathway for insect herbivores adapting to novel host plants. AlthoughA. gossypii born on hibiscus cannot directly colonize cucumber,
it can colonize cucumber through the short feeding experience on
cucumber infected with a biotrophic phytopathogen. Under natural
conditions, possibility of cucumber being infected by phytopathogens
always exists, which provides chances for A. gossypii adapting to
cucumber. Thus, we have figured out the life history of A.
gossypii that infests cucumber (Figure 4).
Cucumber-specialized and cotton-specialized (or hibiscus-specialized)
lineages of A. gossypii were the most studied host specialized
populations in this species. Liu et al. (2002) found nymphs of A.
gossypii from cotton survived for less than 6 d on cucumber, and nymphs
of the aphid from hibiscus survived for less than 4 d on cucumber, and
nymphs of the aphid from cucumber survived for less than 6 d on cotton
either; but nymphs of the aphid from cotton could adapt to hibiscus and
vice versa. A study from Australia indicated the alate adults from
cotton produced significantly less nymphs on cucumber or pumpkin than on
cotton or hibiscus, and the nymphs deposited on cucumber or pumpkin
could not develop to maturity; the alate adults from pumpkin produced
significantly less nymphs on cotton or hibiscus than on cucumber or
pumpkin (Najar-Rodríguez et al. 2009). The existence of fitness
trade-offs in host-associated populations of A. gossypii were
also reported in several other studies, such as Carletto et al. (2009),
Razmjou et al. (2010) and Satar et al. (2013).
Our results were basically in line with the results of those studies.
Although the HI lineage in our study did not die out within a few days
after being transferred to cucumber, they only maintained very low
population growth and their nymphs developed into yellow dwarfs. Even on
natal hosts, A. gossypii developed into yellow dwarfs when the
population density was high (Watt and Hales 1996). However, the yellow
dwarfs of the HI lineage on fresh cucumber were different from those
dwarfs under high population density because they did not inflict damage
symptom to cucumber plant (Figure 1D). The bad performance of the HI
lineage did not improve with the extension of culture time on fresh
cucumber. Therefore, the HI lineage used in the present study showed
high host specialization as reported in other studies.
Host specialization is widespread in polyphagous insect herbivores (Drès
and Mallet 2002). Genetic adaptation and transcriptional adaptation have
been proposed to explain how polyphagous insect herbivores adapt to
diverse host plants (Mathers et al. 2017). Genetically distinct
host-associated populations were reported frequently in aphids. For
example, more than 10 host races with genetic differentiation were
detected in Western Europe populations of Acyrthosiphon pisum(Peccoud et al. 2009). The cotton-melon aphid A. gossypiicollected from different plant families at large geographical scale were
genetically structured by host species (Carletto et al. 2009). In the
sugarcane aphid Melanaphis sacchari , host transfer experiments
demonstrated the existence of fitness trade-offs, and genetic test
revealed genetic structure linked to host plants (Nibouche, et al.
2015). Also, in Myzus persicae , microsatellite DNA analysis
revealed genetic divergence between host-associated populations
(Margaritopoulos et al. 2007). Genetic basis of host-specialized
populations reflected the outcome of long-time coevolution between
insects and host plants. However, a recent study showed that M.
persicae was able to adapt to diverse host plants in the absence of
genetic basis through rapid transcriptional plasticity of genes (Mathers
et al. 2017). The HI lineage of A. gossypii was highly
specialized on hibiscus and cotton, manifesting as high mortality, very
low population growth, abnormal morphology, and more importantly,
inflicting no damage symptom to cucumber plant. The feeding experience
of as short as two generations on the pre-infected cucumber could make
the HI lineage fully adapt to cucumber. We considered that this rapid
adaptation was related to transcriptional adaptation rather than genetic
adaptation. Some genes related to aphid-plant interaction could be
stimulated in this rapid adaptation process.
During feeding, aphid secreted saliva which contained a range of
salivary proteins into plant (Will et al. 2007). Some of them acted as
effectors that inhibited plant defenses, such as preventing sieve
element occlusion (Elzinga et al. 2014; Yates-Stewart et al. 2020; Guo
et al. 2020). Meanwhile, plants could recognize some salivary proteins
to elicit defense responses, which was thought to determine the host
range of aphids (Rodriguez and Bos, 2013; Boulain et al. 2019). Similar
to aphids, biotrophic phytopathogens, such as cucumber downy mildew,P. cubensis , also secreted proteins or metabolites into plants
during infecting to prevent occlusion or apoptosis of sieve element.
Aphids and phytopathogens (especially biotrophic phytopathogens) may
have high similarities in suppressing plant immune response by secreting
proteins or metabolites into plants. The HI lineage of A.
gossypii cannot ingest phloem sap on fresh cucumber but can on
pre-infected cucumber. It is possible that the infection of P.
cubensis disrupted the immune of cucumber cells which facilitated
subsequent phloem sap ingestion of the aphid. That is to say, the HI
lineage of A. gossypii hitchhiked P. cubensis in
overcoming plant defenses. Whether this is the case remains to be
verified.