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Meta-analysis reveals intraspecific variation in herbivores for plant-mediated
interactions
Knegt, 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.; de
Lemos, 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.; SolisVargas, Manuel; Kiers, E. Toby; Egas, C.J.M.
Link to publication
Citation for published version (APA):
Knegt, A. J., Alba Cano, J. M., Silva Ataide, L. M., Barbosa, T. A., Bernardo, A. M. G., Chafi, R., ... Egas, C. J.
M. (2017). Meta-analysis reveals intraspecific variation in herbivores for plant-mediated interactions. Poster
session presented at Gordon Research Conference "Plant - Herbivore Interactions", Ventura, CA, USA, United
States.
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Download date: 17 Jun 2017
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UNIVERSITY OF AMSTERDAM
Bram Knegt ,
1
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
Institute 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.
1
Meta-analysis reveals intraspecific variation for plant-mediated interactions in herbivores
Summary
Introduction
Plant-mediated interactions among herbivores are important drivers of
community dynamics, but we lack insight into variation among herbivores
for these interactions.
When herbivores attack a plant, they induce changes in plant traits, which affect other herbivores on the same plant. Such ‘plant-mediated interactions’ among herbivores are important
drivers of community dynamics (Stam et al. 2014).
A meta-analysis of datasets investigating plant-mediated interactions between 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.
Selection among herbivore populations can produce intraspecific variation for plant-mediated 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:
I
In both interactions effect sizes varied strongly, with 18 - 29% variation explained by the time populations had been cultured. Longer lab culturing
produced smaller effect sizes.
to what extent do the spider mites Tetranychus evansi and Tetranychus urticae affect the performance of other spider mites through plant-mediated effects?
II what factors contribute to variation in the strength of the interaction?
Study system & Experiments
Step 1: infest with T. evansi, T. urticae
or no mites for 2 - 7 days
0.1 mm
Step 2: remove mites, eggs and web
with a fine brush
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
T. urticae (left) and T. evansi (right) adult females
Spider mites are arthropod herbivores that feed
on plant parenchyma cell content. The two-spotted spider mite Tetranychus urticae generally induces a defense response in tomato (Kant et al. 2004,
Martel et al. 2015), whereas the tomato red spider
mite Tetranychus evansi suppresses the tomato defense response (Sarmento et al. 2011, Alba et al. 2015).
Solanum lycopersicum
tomato plant
Materials & Methods
Results
We 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 plants
We used these effect sizes (std mean difference) as input for random-effects meta-analysis.
II
A. T. evansi-infested plants vs. clean control plants
Effect size decreased as populations had been cultured in the lab for longer periods, explaining 18 - 29% of the variation among datasets. The remaining variation
was not explained.
A. T. evansi-infested plants vs. controls
negative interaction
positive interaction
Mean (M) = 0.699
T (23) = 2.52, p = 0.019
Standard deviation (T) = 1.07
Q (23) = 124.19, p < 0.001
B. T. urticae-infested plants vs. controls
F1,22 = 5.53, p = 0.028
2T
F1,22 = 5.88, p = 0.024
-1
6
Effect size (standardized mean difference)
I
T. evansi had positive effects on the performance of other
mites, and T. urticae affected them negatively. Both interactions showed strong variability.
-3.00
M
5.00
10.00
B. T. urticae-infested plants vs. clean control plants
0
-4
-3
2
-2
-1
4
0.00
2T
0
negative interaction
Mean (M) = -0.635
T (23) = -2.58, p = 0.017
Standard deviation (T) = 0.961
Q (23) = 118.43, p < 0.001
-5
50
150
250
350
positive interaction
50
150
250
350
-8.00-
Time in culture (estimated number of generations)
Solid lines indicate model predictions, shaded areas delineate 95% confidence intervals, and circles indicate observed effect size estimates.
Discussion
The reduction in effect size over time can be explained by loss of function due to selection 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.
4.00
2T
2T
M
0.00
3.00
Effect size (standardized mean difference)
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.
Literature cited
Alba, 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 suppress 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 tomato 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 herbivore 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.