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Meta-analysis reveals intraspecific variation in herbivores for plant-mediatedinteractionsKnegt, A.J.; Alba Cano, J.M.; Silva Ataide, L.M.; Barbosa, Tomaz A.; Bernardo, Ana M.G.;Chafi, R.; Dias, C.R.; Duarte, Marcus A.; Godinho, Diogo P.; Janssen, A.R.M.; Kant, M.; deLemos, F.; Mencalha, Jussara; Li, Dan; de Oliveira, Elisa F.; Oliveira, Maria G.A.; Pallini, A.;Ribeiro, Fabricio R.; Schimmel, B.C.J.; da Silva, Pauliana A.; da Silva Junior, Neilier R.; Solis-Vargas, Manuel; Kiers, E.T.; Egas, C.J.M.

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Citation for published version (APA):Knegt, B., Alba, J. M., Ataide, L. M. S., Barbosa, T. A., Bernardo, A. M. G., Chafi, R., ... Egas, M. (2017). Meta-analysis reveals intraspecific variation in herbivores for plant-mediated interactions. Poster session presented atGordon Research Conference "Plant - Herbivore Interactions", Ventura, CA, USA, United States.

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Download date: 11 Nov 2018

Bram Knegt1, Juan M. Alba1, Livia M.S. Ataíde1,2, Tomaz A. Barbosa2, Ana M.G. Bernardo2, Rachid Chafi1, Cleide R. Dias2, Marcus A. Duarte2, Diogo P. Godinho3, Arne Janssen1, Merijn R. Kant1, Felipe Lemos1,2, Jussara Mencalha2, Dan Li1, Elisa F. de Oliveira2, Maria G.A. Oliveira2, Angelo Pallini2, Fabrício R. Ribeiro2, Bernardus C.J. Schimmel1, Pauliana A. da Silva2, Neilier R. da Silva Junior2, Manuel Solis-Vargas2, E. Toby Kiers4 and Martijn Egas1

UNIVERSITY OF AMSTERDAM

bramknegt@gmail.com

1Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, P.O. box 94248, 1090 GE Amsterdam, Netherlands; 2Departamento de Entomologia, Universidade Federal de Viçosa (UFV), CEP 36570-900 Minas Gerais, Viçosa, Brazil; 3cE3c – Centre for Ecology, Evolution and Environmental Changes, University of Lisbon, P-1749016 Lisbon, Portugal; 4Department of Ecological Science, Vrije Universiteit, 1081 HV, Amsterdam, Netherlands.

Meta-analysis reveals intraspecific variation for plant-mediated interactions in herbivores

When herbivores attack a plant, they induce changes in plant traits, which affect other herbi-vores on the same plant. Such ‘plant-mediated interactions’ among herbivores are important drivers of community dynamics (Stam et al. 2014).

Selection among herbivore populations can produce intraspecific variation for plant-mediat-ed interactions with other herbivores. However, few studies assess this variability, which is what we did here, using plant-mediated interactions between two spider mite species on tomato host plants. We ask:

Introduction

Discussion

I

II

to what extent do the spider mites Tetranychus evansi and Tetranychus urticae af-fect the performance of other spider mites through plant-mediated effects?

what factors contribute to variation in the strength of the interaction?

Summary

Materials & MethodsWe found 38 datasets where intact tomato plants were infested with either T. evansi or T. urticae (Step 1), and oviposition rates of other T. evansi or T. urticae populations were measured on the same leaflet (Step 3). For each dataset we calculated the standardized mean difference in oviposition rates per plant of adult females between: A. T. evansi-infested plants and clean control plants B. T. urticae-infested plants and clean control plantsWe used these effect sizes (std mean difference) as input for random-effects meta-analysis.

0.1 mm

T. urticae (left) and T. evansi (right) adult females

Spider mites are arthropod herbivores that feed on plant parenchyma cell content. The two-spot-ted spider mite Tetranychus urticae generally in-duces a defense response in tomato (Kant et al. 2004, Martel et al. 2015), whereas the tomato red spider mite Tetranychus evansi suppresses the tomato de-fense response (Sarmento et al. 2011, Alba et al. 2015).

Solanum lycopersicumtomato plant

Step 2: Step 3: cut leaf discs from damaged tissue, place new adult females on each leaf disc individually, and assess oviposition rate over 2 - 5 days

Step 1: infest with T. evansi, T. urticae or no mites for 2 - 7 days

remove mites, eggs and web with a fine brush

Plant-mediated interactions among herbivores are important drivers of community dynamics, but we lack insight into variation among herbivores for these interactions.

A meta-analysis of datasets investigating plant-mediated interactions be-tween herbivorous Tetranychus urticae and Tetranychus evansi spider mites infesting Solanum lycopersicum tomato plants showed that T. urticae had negative effects on the performance of other spider mite populations, whereas T. evansi affected them positively.

In both interactions effect sizes varied strongly, with 18 - 29% variation ex-plained by the time populations had been cultured. Longer lab culturing produced smaller effect sizes.

Study system & Experiments

Effect size (standardized mean difference)

B. T. urticae-infested plants vs. clean control plants

-8.00- 4.00 0.00 3.00M

2T 2T

Mean (M) = -0.635T (23) = -2.58, p = 0.017Standard deviation (T) = 0.961Q (23) = 118.43, p < 0.001

positive interactionnegative interaction

A. T. evansi-infested plants vs. clean control plants

-3.00 0.00 5.00 10.00M

2T 2T

Mean (M) = 0.699T (23) = 2.52, p = 0.019Standard deviation (T) = 1.07Q (23) = 124.19, p < 0.001

positive interactionnegative interaction

Results

IT. evansi had positive effects on the performance of other mites, and T. urticae affected them negatively. Both interac-tions showed strong variability.

IIEffect size decreased as populations had been cultured in the lab for longer peri-ods, explaining 18 - 29% of the variation among datasets. The remaining variation was not explained.

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Time in culture (estimated number of generations)

F1,22 = 5.53, p = 0.028 F1,22 = 5.88, p = 0.024

A. T. evansi-infested plants vs. controls B. T. urticae-infested plants vs. controls

The reduction in effect size over time can be explained by loss of function due to selec-tion against plant defense induction and suppression in lab cultures, or due to mutation accumulation as a result of random genetic processes.

This case of ‘inadvertent selection’ in lab cultures demonstrates intraspecific variation in herbivores for plant-mediated effects on other herbivoves, and suggests a change in heritable variation for these interactions over time.

Literature citedAlba, J.M., Schimmel, B.C.J., Glas, J.J., Ataide, L.M.S., Pappas, M.L., Villarroel, C.A., Schuurink, R.C., Sabelis, M.W. & Kant, M.R. (2015) Spider mites sup-

press tomato defences downstream of jasmonate and salicylate independently of hormonal crosstalk. New Phytologist, 205, 828-840.Kant, M.R., Ament, K., Sabelis, M.W., Haring, M.A. & Schuurink, R.C. (2004) Differential timing of spider mite-induced direct and indirect defences in to-

mato plants. Plant Physiology, 135, 483-495.Martel, C., Zhurov, V., Navarro, M., Martinez, M., Cazaux, M., Auger, P., Migeon, A., Santamaria, M.E., Wybouw, N., Diaz, I., Van Leeuwen, T., Navajas, M.,

Grbic, M. & Grbic, V. (2015) Tomato whole genome transcriptional response to Tetranychus urticae identifies divergence of spider mite-induced responses between tomato and Arabidopsis. Molecular Plant-Microbe Interactions, 28, 343-361.

Sarmento, R.A., Lemos, F., Bleeker, P.M., Schuurink, R.C., Pallini, A., Oliveira, M.G.A., Lima, E.R., Kant, M.R., Sabelis, M.W. & Janssen, A. (2011) A herbi-vore that manipulates plant defence. Ecology Letters, 14, 229-236.

Stam, J.M., Kroes, A., Li, Y., Gols, R., van Loon, J.J.A., Poelman, E.H. & Dicke, M. (2014). Plant interactions with multiple insect herbivores: from community to genes. Annual Review of Plant Biology, 65, 689-713.

Effect sizes are indicated by filled squares, and error bars represent their 95% confidence intervals. The estimated summary effect is represented by a diamond, of which the vertical extremes indicate the summary effect size and the horizontal extremes the 95% confidence interval. The error bars next to the diamond indicate the 95% prediction interval.

Solid lines indicate model predictions, shaded areas delineate 95% confidence intervals, and circles indicate observed effect size estimates.