Collapse of obligate endosymbiosis in selfed progeny of the pea aphid, Acyrthosiphon pisum

The relationship between inbreeding depression and microbial endosymbiosis in animals has been largely overlooked, despite their widespread occurrence. Aphids host the intracellular symbiotic bacterium Buchnera aphidicola, which provides them with nutrition and is vertically transmitted to offspring. Experimental elimination of Buchnera results in host sterility. We previously observed such sterility in the selfed progeny of the pea aphid, Acyrthosiphon pisum. In the present study, we tested our hypothesis that selfing disrupts aphid–Buchnera endosymbiosis and leads to sterile fundatrices in A. pisum. Initially, we performed crossing experiments involving nine strains, revealing widespread sterility in A. pisum. Subsequently, we selected two strains for more detailed analyses, including quantification of relative Buchnera genome copy numbers and fluorescent in situ hybridization of Buchnera. Fundatrices resulting from selfing in one strain exhibited reduced fecundity and diminished Buchnera abundance compared with those resulting from outcrosses. These findings represent the first example of inbreeding depression impacting endosymbiotic abundance in animal–microbe symbiosis. Furthermore, fecundity was positively correlated with Buchnera abundance in selfed progenies. Overall, these results suggest that inbreeding negatively affects insects through endosymbiosis collapse.