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A genetic basis for the manipulation of sink–source relationships by the galling aphid Pemphigus batae

  • Plant-Animal interactions - Original Paper
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Abstract

We examined how the galling aphid Pemphigus batae manipulates resource translocation patterns of resistant and susceptible narrowleaf cottonwood Populus angustifolia. Using carbon-14 (14C)-labeling experiments in common garden trials, five patterns emerged. First, although aphid galls on resistant and susceptible genotypes did not differ in their capacity to intercept assimilates exported from the leaf they occupied, aphids sequestered 5.8-fold more assimilates from surrounding leaves on susceptible tree genotypes compared to resistant genotypes. Second, gall sinks on the same side of a shoot as a labeled leaf were 3.4-fold stronger than gall sinks on the opposite side of a shoot, which agrees with patterns of vascular connections among leaves of the same shoot (orthostichy). Third, plant genetic-based traits accounted for 26% of the variation in sink strength of gall sinks and 41% of the variation in sink strength of a plant’s own bud sinks. Fourth, tree susceptibility to aphid gall formation accounted for 63% of the variation in 14C import, suggesting strong genetic control of sink–source relationships. Fifth, competition between two galls was observed on a susceptible but not a resistant tree. On the susceptible tree distal aphids intercepted 1.5-fold more 14C from the occupied leaf than did basal aphids, but basal aphids compensated for the presence of a distal competitor by almost doubling import to the gall from surrounding leaves. These findings and others, aimed at identifying candidate genes for resistance, argue the importance of including plant genetics in future studies of the manipulation of translocation patterns by phytophageous insects.

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Acknowledgments

We are especially grateful to R. Dickson, J. Isebrands, and P. Larson of the Forest Service Laboratory in Rhinelander, WI, for sharing with us their 14C-labeling techniques on eastern cottonwood and providing critical advice for this study. We thank D. Kimberling, L. Von der Heydt, and R. Pantera for assistance in the laboratory and T. Craig, G. Fernandez, D. Gettinger, J. Itami, M. Kearsley, N. Moran, and C. Sacchi for advice during the study. R. Foust provided laboratory space. This research was supported by the National Science Foundation, Sigma Xi, the Bilby Research Center and Organized Research of Northern Arizona University, the Merriam-Powell Center for Environmental Research, and the Utah Power and Light Co.

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Authors and Affiliations

  1. Cottonwood Ecology Group, Department of Biology, Northern Arizona University, Flagstaff, AZ, 86011-5640, USA

    Zacchaeus G. Compson, Matthew S. Zinkgraf & Thomas G. Whitham

  2. Department of Biology, University of Central Arkansas, Conway, AR, 72035, USA

    Katherine C. Larson

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  1. Zacchaeus G. Compson
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  2. Katherine C. Larson
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  3. Matthew S. Zinkgraf
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  4. Thomas G. Whitham
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Correspondence to Zacchaeus G. Compson.

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Communicated by Colin Orians.

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Compson, Z.G., Larson, K.C., Zinkgraf, M.S. et al. A genetic basis for the manipulation of sink–source relationships by the galling aphid Pemphigus batae . Oecologia 167, 711–721 (2011). https://doi.org/10.1007/s00442-011-2033-x

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