A tale of two symbionts: Bacterial facilitation versus restriction of host plant use by Aphis craccivora

Facultative bacterial endosymbionts are maternally inherited microbes that can confer beneficial traits to insects but are not required for host survival. In polyphagous herbivorous insects, populations found on different host plants are often infected with different facultative endosymbionts. It is possible that endosymbionts are directly responsible for plant specialization and/or host race formation in these instances, but this hypothesis has only been tested in the pea aphid, with inconclusive results. My objective is to test whether endosymbionts influence host plant use by the polyphagous aphid, Aphis craccivora. Aphis craccivora found on Robinia pseudoacacia (black locust) is predominantly infected with the facultative endosymbiont Arsenophonus, whereas aphids found on Medicago sativa (alfalfa) are predominantly infected with the endosymbiont Hamiltonella. I tested whether either endosymbiont differentially affects aphid fitness across three host plants using naturally infected versus antibiotic cured colonies of A. craccivora.  In greenhouse and field studies, I found that Arsenophonus increased aphid population growth 1.6 to 5.3 fold relative to cured colonies on black locust, but decreased growth by 59 to 67% on alfalfa and fava. In contrast, Hamiltonella decreased aphid population growth on all tested plants, and was particularly costly on black locust where infected aphid populations had negative growth rates.  Hamiltonella-cured aphids had positive growth rates equivalent to Arsenophonus-cured aphids on black locust. Thus, removing both symbionts equalized performance of two aphid lineages that otherwise would be considered host races. In conclusion facultative endosymbionts are responsible for host specialization and apparent host race formation in A. craccivora.