Last week in the Plant-Interactions-Group we had our 3rd JIGSAW session. Our topic was specialists vs. generalists in plant-herbivore interactions. I was inspired to cover this topic because it is a persistent issue, one that has been discussed widely in ecology for decades. Are specialists and generalists fundamentally different in their ecological and evolutionary relationships with plants? Is this an important predictive axis to test hypotheses? Addressing this was, in part, also motivated by last week’s Agrawal lab meeting, where we invited Emeritus Professor Paul Feeny to join and discuss some of the classic research that came out of his lab in the 1970s. One of the papers we discussed was Blau et al. (1978, Science): “Allylglucosinolate and herbivorous caterpillars – contrast in toxicity and tolerance”. In that highly cited study, Paul’s lab demonstrated how glucosinolates (compounds characteristic of the mustard family, Brassicaceae) are least toxic to Pieris rapae (caterpillar of the cabbage white, a specialist on mustards), somewhat toxic at high concentrations to a generalist caterpillar Spodoptera, and the most toxic to a specialist swallowtail caterpillar (specialized on plants outside the mustard family).
Since then, much has been made of specialists versus generalists. And some important generalities have emerged. For example, Lee Dyer’s groundbreaking study (1995, Ecology): “Tasty generalists and nasty specialists? Antipredator mechanisms in tropical lepidopteran larvae”, empirically cemented the notion that specialist caterpillars are better defended against their predators than generalist caterpillars, often due to chemistry sequestered from host plants. Other predictions, such as that which grew out of Blau et al., that adapted specialists should be less impacted by “defense” chemicals than generalists has been born out of meta-analyses (e.g., Cornell and Hawkins, 2003, Am Nat, “Herbivore responses to plant secondary compounds: A test of phytochemical coevolution theory”). Nonetheless, other hypotheses and predictions have been less well-tested or supported. For example, do specialists induce different plant responses than generalists when attacking plants? Do specialists versus generalists impose different patterns of selection on plants? And do specialists versus generalists show different patterns of herbivory along ecological gradients such as latitude?
We read three recent papers and discussed their relevance to conceptual issues of specialists versus generalists as well as their relationship to each other. In the first, Rick Lankau conducted a study estimating natural selection by a specialist aphid vs. a generalist slug in the field. He did this work while a graduate student at UC Davis. Indeed, glucosinolates were favored in the presence of the generalist, but not in the presence of the specialist. In the next study, Daniel Anstett, a graduate student in Marc Johnson’s lab at the University of Toronto, showed that along an expansive latitudinal gradient, herbivory on the common evening primrose (Oenothera biennis) was differentially impacted by herbivores. The study was a spectacular effort, with tremendous sampling all along the plant’s full range across eastern North America. Although generalist leaf chewers did not show a pattern of increasing or decreasing damage wit latitude, a specialist bud galling moth and a free-living fruit-eating moth both increased there damage at higher latitudes (moving north) from Florida. Nonetheless, a third specialist, in this case a beetle, whose larvae feed in the stem tissue, showed the opposite pattern, with decreasing herbivory moving north. These distinct patterns showed that specialists and generalists did not behave the same along this population-level gradient. Perhaps their own distributions followed a latitudinal pattern, due to climate or availability of this (or alternate) host plants?
In the final study, Bidart-Bouzat and Kliebenstein tested the impact of feeding by three specialists (2 Lepidoptera and an aphid) and three generalists (also 2 leps and an aphid) on gene expression and glucosinolate production of Arabidopsis. This beautifully designed study had real replication in pairs of related specialists and generalists from two feeding guilds. Overall specialists did not cause predictably different plant responses than generalists. Although it would be nice if the world worked cleanly enough for specialists and generalists to cause differential induced plant responses, the specific evolutionary relationships that each species has with the plant is likely more important.
Rules for how specialists and generalists interact with plants are still a ways away from being codified. Strong experimental designs, with replicated specialist and generalist species, and considering their taxonomy is critical. The choice of species, and how specialized they are (to one plant species, a plant genus, or the whole botanical family) is likely to be important. Lab-rat generalists like Spodoptera are a favorite for many reasons, but are they representative? Different levels of analysis (natural selection on genotypes, relationships among different populations, and plastic responses in a single plant genotype) are not likely to show the same patterns, and we should be clear about what hypothesis is being tested at whatever level of analysis.
And finally, as a student pointed out in the discussion, one generality emerged from the three papers and their discussion: The feeding guild was extremely important in all cases. In the Arabidopsis study, the two aphids clearly caused much more similar plant responses than the four lepidopteran larvae. In the other two studies, the specialists and generalists were confounded by belonging to different guilds. The feeding mode is likely very important in the ecology and evolution of plant-insect interactions. This makes sense: feeding guild dictates the type of feeding, what tissues are punctured and consumed, and must be a coarser distinction than specialist versus generalist. Incidentally, the late Professor Dick Root, a founding member of the Cornell plant-insect interactions community defined the concept of “feeding guild”. He defined guild as a group of species that utilize the same resource in the same way. Chewing caterpillars versus sucking aphids would certainly fall into two of Root’s plant-feeding guilds.