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Host Plant Specialization Governed by Facultative Symbiont

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Science  26 Mar 2004:
Vol. 303, Issue 5666, pp. 1989
DOI: 10.1126/science.1094611

In North America and Europe, the pea aphid (Acyrthosiphon pisum) encompasses ecologically and genetically distinct host races, offering a model system for studies on sympatric speciation (1, 2). One host race lives on red clover (Trifolium pratense) and cannot produce offspring on alfalfa (Medicago sativum). The other race lives on alfalfa and produces few offspring on red clover. This instance of host plant specialization was attributed to chromosomal loci of the aphid (1), but we report that in Japan, host plant specialization of pea aphid is strongly affected by a facultative endo-symbiotic bacterium.

In Japan, pea aphids feed mainly on vetch (Vicia sativa) and white clover (Trifolium repens) (Fig. 1A) and are able to reproduce on both. Although red clover and alfalfa are found in Japan, indigenous pea aphids rarely utilize these plants [supporting online material (SOM) SOM text]. Pea aphids in natural Japanese populations exhibited a characteristic geographical distribution of endosymbiont infection with a facultative γ-proteobacterium, called pea aphid U-type symbiont (PAUS) (3). The endosymbiont was more common in northern regions where vetch plants are rare (fig. S1). At three locations in central Japan where vetch and white clover are sympatrically available, the occurrence of PAUS was consistently higher on white clover than on vetch (fig. S2).

Fig. 1.

(A) Pea aphid and host plants. [Photos courtesy of K. Tamukai and S. Aoki] (B) Performance of PAUS-infected and uninfected aphids on vetch and white clover. (Top) Naturally PAUS-infected strain TUtdw (orange, n = 14 for vetch and n = 17 for clover) and PAUS-eliminated strain TUtamp (green, n = 10 for vetch and n = 15 for clover). (Bottom) PAUS-eliminated strain TUtamp/TUtamp (green, n = 11 for vetch and n = 12 for clover), and PAUS-reintroduced strain TUtamp/TUt (orange, n = 16 for vetch and n = 18 for clover). Values are mean ± SD. Asterisks indicate statistically significant differences (Mann-Whitney U test: *, P < 0.05; **, P < 0.01; ***, P < 0.001).

We generated aphid strains that are genetically identical and differ only in PAUS infection (4). Adult aphids of a naturally PAUS-infected strain, TUt, were injected with ampicillin at a dose of 1 μg/mg body weight, which selectively eliminated PAUS from their offspring without affecting the essential symbiont Buchnera. Using this technique (5), we obtained a PAUS-free strain, TUtamp, and a PAUS-infected control strain, TUtdw, which had been injected with distilled water instead of the antibiotic. Whereas these strains exhibited similar levels of fecundity on vetch, the PAUS-eliminated strain lost almost 50% fecundity compared with the infected strain on white clover (Fig. 1B, top).

We reintroduced PAUS into the TUtamp strain by injecting hemolymph from the infected strain TUt, to generate an infected strain TUtamp/TUt. A control uninfected strain TUtamp/TUtamp was prepared by injecting hemolymph from TUtamp into the same strain TUtamp. The reintroduction of PAUS resulted in an almost complete recovery of fecundity in the recipient aphids on white clover (Fig. 1B, bottom).

These results indicate that PAUS infection improves the fitness of the host aphid specifically on white clover. An association between PAUS infection and white clover has been reported from pea aphids in California (6) and between PAUS infection and red clover in France (2). Hence, the plant-specific fitness effect of PAUS infection may be not restricted to Japanese populations of the aphid.

Our finding does not necessarily contradict the notion that nuclear genes of the insect play a major role in determining its ecological traits, including plant specialization (1, 2). It appears likely that the effect of the symbiont is also affected by the host genotype. However, this discovery would shed new light on some aspects in evolutionary ecology of aphids and other herbivores, including host race, ecotype, and sympatric speciation.

Supporting Online Material

www.sciencemag.org/cgi/content/full/303/5666/1989/DC1

Materials and Methods

SOM Text

Figs. S1 and S2

References

References and Notes

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