Effect of Host Genotype on Symbiont Titer in the Aphid—Buchnera Symbiosis

Abstract: Obligate nutritional symbioses require balance between the energetic needs of the host and the symbiont. The resident symbiont population size within a host may have major impacts on host fitness, as both host and symbiont consume and supply metabolites in a shared metabolite pool. Given the massive genome degradation that is a hallmark of bacterial endosymbionts of insects, it is unclear at what level these populations are regulated, and how regulation varies among hosts within natural populations. We measured the titer of the endosymbiont Buchnera aphidicola from different clones of the pea aphid, Acyrthosiphon pisum, and found significant variation in titer, measured as Buchnera genomes per aphid genome, among aphid clones. Additionally, we found that titer can change with the age of the host, and that the number of bacteriocytes within an aphid is one factor likely controlling Buchnera titer. Buchnera titer measurements in clones from a sexual cross indicate that the symbiont genotype is not responsible for variation in titer and that this phenotype is likely non-heritable across sexual reproduction. Symbiont titer is more variable among lab-produced F₁ aphid clones than among field-collected ones, suggesting that intermediate titer is favored in natural populations. Potentially, a low heritability of titer during the sexual phase may generate clones with extreme and maladaptive titers each season.