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Simple Summary: The cotton-melon aphid, Aphis gossypii Glover, is a polyphagous insect pest with many host-specialized biotypes. The mechanism of host specificity remains unknown in this aphid. In this study, we investigated whether bacterial symbionts control the host specificity of A. gossypii, as reported in some aphids. The two typical host-specialized biotypes used in this study produced significantly fewer nymphs on non-native hosts than on a native host, indicating a high host specificity of the two biotypes. We found that the winged morph of both biotypes had a significantly lower host specificity than its corresponding wingless morph. Bacterial analysis indicated that the composition of the bacterial symbionts was not different between the two biotypes, but within each biotype, the Buchnera abundance in the winged morph was only about 10% of that in the wingless morph. We suspected that a low Buchnera abundance was associated with a low host specificity. We compared the reproduction of A. gossypii with different Buchnera abundances, and did not find that a low Buchnera abundance resulted in a low host specificity. We then concluded that the host specificity of A. gossypii is not controlled by specific bacterial symbionts or Buchnera abundance. The cotton-melon aphid, Aphis gossypii Glover, is a polyphagous insect pest with many host-specialized biotypes, such as the Cucurbitaceae- and Malvaceae-specialized (CU and MA) biotypes. Bacterial symbionts were reported to determine the host range in some aphids. Whether this is the case in A. gossypii remains unknown. Here, we tested the host specificity of the CU and MA biotypes, compared the host specificity between the wingless and winged morph within the same biotype, and analyzed the composition of the bacterial symbionts. The reproduction of the CU and MA biotypes reduced by 66.67% and 82.79%, respectively, on non-native hosts, compared with on native hosts. The composition of bacterial symbionts was not significantly different between the CU and MA biotypes, with a Buchnera abundance >95% in both biotypes. Meanwhile, the winged morph produced significantly more nymphs than the wingless morph on non-native hosts, and the Buchnera abundance in the winged morph was only about 10% of that in the wingless morph. There seemed to be a relationship between the Buchnera abundance and host specificity. We regulated the Buchnera abundance by temperature and antibiotics, but did not find that a low Buchnera abundance resulted in the high reproduction on non-native hosts. We conclude that the host specificity of A. gossypii is not controlled by specific bacterial symbionts or by Buchnera abundance. [ABSTRACT FROM AUTHOR]

Polyphagous aphids often consist of host‐specialized lineages, which have greater fitness on their native hosts than on others. The underlying causes are important for understanding of the evolution of diet breadth and host shift of aphids. The cotton‐melon aphid Aphis gossypii Glover is extremely polyphagous with many strict host‐specialized lineages. Whether and how the lineage specialized on the primary host hibiscus shifts to the secondary host cucumber remains elusive. We found that the hibiscus‐specialized lineage suffered high mortality and gave birth to very few nymphs developing into yellow dwarfs on fresh cucumber leaves, and did not inflict any damage symptoms on cucumber plants. The poor performance did not improve with prolonged exposure to cucumber; however, it did significantly improve when the cucumber leaves were pre‐infected with a biotrophic phytopathogen Pseudoperonospora cubensis. More importantly, the hibiscus‐specialized lineage with two‐generation feeding experience on pre‐infected cucumber leaves performed as well as the cucumber‐specialized lineage did on fresh cucumber leaves, and inflicted typical damage symptoms on intact cucumber plants. Electrical penetration graph (EPG) indicated that the hibiscus‐specialized lineage did not ingest phloem sap from fresh cucumber leaves but succeeded in ingesting phloem sap from pre‐infected cucumber leaves, which explained the performance improvement of the hibiscus‐specialized lineage on pre‐infected cucumber leaves. This study revealed a new pathway for the hibiscus‐specialized lineage to quickly acclimate to cucumber under the assistance of the phytopathogen. We considered that the short feeding experience on pre‐infected cucumber may activate expression of effector genes that are related to specific host utilization. We suggest to identify host‐specific effectors by comparing proteomes or/and transcriptomes of the hibiscus‐specialized lineage before and after acclimating to cucumber. [ABSTRACT FROM AUTHOR]