Tell me what you’ve eaten, I’ll tell you how much you’ll eat (and be eaten)
Intraspecific difference among herbivore lineages and their host-plant specialization drive the strength of trophic cascades
Tritrophic interactions have a central role in ecological theory and applications [1-3]. Particularly, systems comprised of plants, herbivores and predators have historically received wide attention given their ubiquity and economic importance . Although ecologists have long aimed to understand the forces that govern alternating ecological effects at successive trophic levels , several key open questions remain (at least partially) unanswered . In particular, the analysis of complex food webs has questioned whether ecosystems can be viewed as a series of trophic chains [7,8]. Moreover, whether systems are mostly controlled by top-down (trophic cascades) or bottom-up processes remains an open question .
Traditionally, studies have addressed how species diversity at different food chain compartments affect the strength and direction of trophic cascades . For example, many studies have tested whether biological control was more efficient with more than one species of natural enemies [10-12]. Much less attention has been given to the role of within-species variation in shaping trophic cascades . In particular, whereas the impact of trait variation within species of plants or predators on successive trophic levels has been recently addressed [14,15], the impact of intraspecific herbivore variation is in its infancy (but see ). This is at odds with the resurgent acknowledgment of the importance of individual variation for several ecological processes operating at higher levels of biological organization .
Sources of variation within species can come in many flavours. In herbivores, striking ecological variation can be found among populations occurring on different host plants, which become genetically differentiated, thus forming host races [18,19]. Curiously, the impact of variation across host races on the strength of trophic cascades has, to date, not been explored. This is the gap that the manuscript by Sentis and colleagues  fills. They experimentally studied a curious tri-trophic system where the primary consumer, pea aphids, specializes in different plant hosts, creating intraspecific variation across biotypes. Interestingly, there is also ecological variation across lineages from the same biotype. The authors set up experimental food chains, where pea aphids from different lineages and biotypes were placed in their universal legume host (broad bean plants) and then exposed to a voracious but charming predator, ladybugs. The full factorial design of this experiment allowed the authors to measure vertical effects of intraspecific variation in herbivores on both plant productivity (top-down) and predator individual growth (bottom-up).
The results nicely uncover the mechanisms by which intraspecific differences in herbivores precipitates vertical modulation in food chains. Herbivore lineage and host-plant specialization shaped the strength of trophic cascades, but curiously these effects were not modulated by density-dependence. Further, ladybugs consuming pea aphids from different lineages and biotypes grew at distinct rates, revealing bottom-up effects of intraspecific variation in herbivores.
These findings are novel and exciting for several reasons. First, they show how intraspecific variation in intermediate food chain compartments can simultaneously reverberate both top-down and bottom-up effects. Second, they bring an evolutionary facet to the understanding of trophic cascades, providing valuable insights on how genetically differentiated populations play particular ecological roles in food webs. Finally, Sentis and colleagues’ findings  have critical implications well beyond their study systems. From an applied perspective, they provide an evident instance on how consumers’ evolutionary specialization matters for their role in ecosystems processes (e.g. plant biomass production, predator conversion rate), which has key consequences for biological control initiatives and invasive species management. From a conceptual standpoint, their results ignite the still neglected value of intraspecific variation (driven by evolution) in modulating the functioning of food webs, which is a promising avenue for future theoretical and empirical studies.
 Price, P. W., Bouton, C. E., Gross, P., McPheron, B. A., Thompson, J. N., & Weis, A. E. (1980). Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annual review of Ecology and Systematics, 11(1), 41-65. doi: 10.1146/annurev.es.11.110180.000353
 Olff, H., Brown, V.K. & Drent, R.H. (1999). Herbivores: between plants and predators. Blackwell Science, Oxford.
 Tscharntke, T. & Hawkins, B.A. (2002). Multitrophic level interactions. Cambridge University Press. doi: 10.1017/CBO9780511542190
 Agrawal, A. A. (2000). Mechanisms, ecological consequences and agricultural implications of tri-trophic interactions. Current opinion in plant biology, 3(4), 329-335. doi: 10.1016/S1369-5266(00)00089-3
 Pace, M. L., Cole, J. J., Carpenter, S. R., & Kitchell, J. F. (1999). Trophic cascades revealed in diverse ecosystems. Trends in ecology & evolution, 14(12), 483-488. doi: 10.1016/S0169-5347(99)01723-1
 Abdala‐Roberts, L., Puentes, A., Finke, D. L., Marquis, R. J., Montserrat, M., Poelman, E. H., ... & Mooney, K. (2019). Tri‐trophic interactions: bridging species, communities and ecosystems. Ecology letters, 22(12), 2151-2167. doi: 10.1111/ele.13392
 Polis, G.A. & Winemiller, K.O. (1996). Food webs. Integration of patterns and dynamics. Chapmann & Hall, New York. doi: 10.1007/978-1-4615-7007-3
 Torres‐Campos, I., Magalhães, S., Moya‐Laraño, J., & Montserrat, M. (2020). The return of the trophic chain: Fundamental vs. realized interactions in a simple arthropod food web. Functional Ecology, 34(2), 521-533. doi: 10.1111/1365-2435.13470
 Polis, G. A., Sears, A. L., Huxel, G. R., Strong, D. R., & Maron, J. (2000). When is a trophic cascade a trophic cascade?. Trends in Ecology & Evolution, 15(11), 473-475. doi: 10.1016/S0169-5347(00)01971-6
 Sih, A., Englund, G., & Wooster, D. (1998). Emergent impacts of multiple predators on prey. Trends in ecology & evolution, 13(9), 350-355. doi: 10.1016/S0169-5347(98)01437-2
 Diehl, E., Sereda, E., Wolters, V., & Birkhofer, K. (2013). Effects of predator specialization, host plant and climate on biological control of aphids by natural enemies: a meta‐analysis. Journal of Applied Ecology, 50(1), 262-270. doi: 10.1111/1365-2664.12032
 Snyder, W. E. (2019). Give predators a complement: conserving natural enemy biodiversity to improve biocontrol. Biological control, 135, 73-82. doi: 10.1016/j.biocontrol.2019.04.017
 Des Roches, S., Post, D. M., Turley, N. E., Bailey, J. K., Hendry, A. P., Kinnison, M. T., ... & Palkovacs, E. P. (2018). The ecological importance of intraspecific variation. Nature Ecology & Evolution, 2(1), 57-64. doi: 10.1038/s41559-017-0402-5
 Bustos‐Segura, C., Poelman, E. H., Reichelt, M., Gershenzon, J., & Gols, R. (2017). Intraspecific chemical diversity among neighbouring plants correlates positively with plant size and herbivore load but negatively with herbivore damage. Ecology Letters, 20(1), 87-97. doi: 10.1111/ele.12713
 Start, D., & Gilbert, B. (2017). Predator personality structures prey communities and trophic cascades. Ecology letters, 20(3), 366-374. doi: 10.1111/ele.12735
 Turcotte, M. M., Reznick, D. N., & Daniel Hare, J. (2013). Experimental test of an eco-evolutionary dynamic feedback loop between evolution and population density in the green peach aphid. The American Naturalist, 181(S1), S46-S57. doi: 10.1086/668078
 Bolnick, D. I., Amarasekare, P., Araújo, M. S., Bürger, R., Levine, J. M., Novak, M., ... & Vasseur, D. A. (2011). Why intraspecific trait variation matters in community ecology. Trends in ecology & evolution, 26(4), 183-192. doi: 10.1016/j.tree.2011.01.009
 Drès, M., & Mallet, J. (2002). Host races in plant–feeding insects and their importance in sympatric speciation. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 357(1420), 471-492. doi: 10.1098/rstb.2002.1059
 Magalhães, S., Forbes, M. R., Skoracka, A., Osakabe, M., Chevillon, C., & McCoy, K. D. (2007). Host race formation in the Acari. Experimental and Applied Acarology, 42(4), 225-238. doi: 10.1007/s10493-007-9091-0
 Sentis, A., Bertram, R., Dardenne, N., Simon, J.-C., Magro, A., Pujol, B., Danchin, E. and J.-L. Hemptinne (2020) Intraspecific difference among herbivore lineages and their host-plant specialization drive the strength of trophic cascades. bioRxiv, 722140, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/722140
Sara Magalhães and Raul Costa-Pereira (2020) Tell me what you’ve eaten, I’ll tell you how much you’ll eat (and be eaten). Peer Community in Ecology, 100047. 10.24072/pci.ecology.100047
Evaluation round #2
DOI or URL of the preprint: 10.1101/722140
Version of the preprint: 1
Author's Reply, None
Decision by Sara Magalhães, 02 Mar 2020
I am now ready to make a recommendation of this preprint. I urge the authors to perform the small modifications requested by the reviewers while I prepare my text! thanks sara
Reviewed by anonymous reviewer, 20 Jan 2020
Reviewed by Bastien Castagneyrol, 18 Feb 2020
Evaluation round #1
DOI or URL of the preprint: https://doi.org/10.1101/722140
Author's Reply, None
Decision by Sara Magalhães, 28 Oct 2019
First of all, I deeply apologize for having taken so long with this reviewing process. Most of the time was spent trying to find reviewers that would agree on reviewing, although I admit that part of the blame is on me too…
In any case, we have received two reviews that I find very helpful. As you will see, both reviewers are overall very positive about your paper, but they also raise some very pertinent issues. I also liked this paper very much, it is very clearly written and the experiments are elegant. However, I totally agree with the referees’ comments and urge you to modify the article accordingly. I herewith state my main comments on the article (note that these are mostly the reviewers comments stated otherwise):
- I agree with the second reviewer that stating “intraspecific variation drives trophic cascades” (cf. title) is misleading. But I see this from a different angle. In my opinion, to test whether intraspecific variation affect trophic cascades you would need to have treatments with more or less intraspecific variation. This was not the case. So you do show that there is intraspecific variation in the ability of aphids to modulate trophic cascades, but you don’t show that the amount of variation matters. As the second reviewer, I still think your question is interesting, but it should be formulated in a less ambiguous fashion.
- I also agree with the first reviewer that there is no clear reason to state that you are testing the role of “evolutionary divergence”. First, I do not see evidence for the fact that alfafa lineages have diverged more from clover lineages than from each other. Indeed, there can be very distantly related lineages within the same host race. Second, I also think that lineages from different plants should be considered as a special case of different lineages in general. In particular, the statistical analysis should reflect this. That is, there should be one statistical model that includes lineage in general, and then specific planned comparisons to compare between host races in particular. I would say this is a more elegant way of analysing the data.
- Finally, I agree with the first reviewer that assessing the effect of each lineage on the strength of the trophic cascade requires a specific test that was not performed, if I understand the stats well. That is, it is tested whether, for each lineage, there is a trophic cascade, but not whether these cascades differ in strength.
- I found that the introduction could be a bit streamlined. In particular, you refer to intraspecific variation in the middle of the second, then in the end of the third paragraph. I would move the former (lines 60-62) to just before the latter. Also, you mention that the role of intraspecific variation for the occurrence of trophic cascades has been studied before. It would be nice to know in which way the current study adds to the available literature. From what I gathered with the references you cited (and check also Clegg 2018 Ecology and Weiss and Post 2013 Oikos) it should be relatively easy to single out your original contribution. But this should be explicitly stated.
- Line 83: change to “the faster their growth, the stronger the trophic cascade”.
- Lines 381-388: basically, I guess that what you’re trying to say is that aphids from Clover may have a lower assimilation efficiency. That is, they eat more (thus impact more the plant) but their conversion into eggs is lower. Right?
- In the Discussion, I think you need to come up with one or more explanations for the differences found between the effects of clover vs alfalfa trophic chains. For example, the fact that ladybeetles are bigger when fed on alfalfa aphids suggest that these are of better quality, which goes in line with my previous point. Also, the fact that alfalfa aphids reach higher densities on this plant (in absence of predators) suggest that there are better adapted than clover aphids. This should be discussed.