Host Plant Determines the Population Size of an Obligate Symbiont (Buchnera aphidicola) in Aphids

Abstract

Buchnera aphidicolais an obligate endosymbiont that provides aphids with several essential nutrients. Though much is known about aphid-Buchnera interactions, the effect of the host plant on Buchnera population size remains unclear. Here we used quantitative PCR (qPCR) techniques to explore the effects of the host plant on Buchnera densities in the cotton-melon aphid, Aphis gossypii Buchneratiters were significantly higher in populations that had been reared on cucumber for over 10 years than in populations maintained on cotton for a similar length of time. Aphids collected in the wild from hibiscus and zucchini harbored more Buchnera symbionts than those collected from cucumber and cotton. The effect of aphid genotype on the population size of Buchnera depended on the host plant upon which they fed. When aphids from populations maintained on cucumber or cotton were transferred to novel host plants, host survival and Buchnera population size fluctuated markedly for the first two generations before becoming relatively stable in the third and later generations. Host plant extracts from cucumber, pumpkin, zucchini, and cowpea added to artificial diets led to a significant increase in Buchnera titers in the aphids from the population reared on cotton, while plant extracts from cotton and zucchini led to a decrease in Buchnera titers in the aphids reared on cucumber. Gossypol, a secondary metabolite from cotton, suppressed Buchnera populations in populations from both cotton and cucumber, while cucurbitacin from cucurbit plants led to higher densities. Together, the results suggest that host plants influence Buchnera population processes and that this may provide phenotypic plasticity in host plant use for clonal aphids.

FIG 1

Bacteriocyte number (A) and relative copy number of the Buchnera aphidicola 16S rRNA gene compared to the aphid ef1a gene (mean ± standard error [SE]; n = 4) from A. gossypii populations maintained on cotton or cucumber (B) and from natural populations collected from cotton, hibiscus, cucumber and zucchini (C). **, significant difference between the cotton and cucumber population aphids at P = 0.01. The different letters indicate significant differences among aphids from the four host plants (P = 0.05, Tukey test).

FIG 2

Relative copy number of the Buchnera aphidicola 16S rRNA gene compared to the aphid ef1a gene in four genotypes of A. gossypii reared on zucchini, cucumber, and cowpea for six generations. The different lowercase letters above the bars indicate significant differences among aphid genotypes on the same host plant (P = 0.05, Tukey test).

FIG 3

Relative copy number of the Buchnera aphidicola 16S rRNA gene compared to the aphid ef1a gene (A and B) and survival rate (C and D) of the aphids from the populations maintained on cotton (A and C) and on cucumber (B and D) reared for different numbers of generations on four host plants.

FIG 4

Relative copy number of the Buchnera aphidicola 16S rRNA gene compared to that of the aphid ef1a gene in the aphids from the populations maintained on cotton (A) and cucumber (B) when fed an artificial diet containing different concentrations of leaf extract from cucumber, cowpea, pumpkin, zucchini, and cotton.

FIG 5

Relative copy number of the Buchnera aphidicola 16S rRNA gene compared to that of the aphid ef1a gene in the aphids from the populations maintained on cotton (A and B) and cucumber (C and D) when fed on artificial diet containing concentrations of 0 to 50 ppm of the plant secondary metabolites gossypol (A and C) and cucurbitacin (B and D) for 0.5, 1, 3, and 5 days. A diet without plant secondary metabolites (0 ppm) was the control.