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Frontiers in chemical ecology and
coevolution
7th New Phytologist Workshop in Ithaca, NY, USA,
September 2013
There has been tremendous growth in the area of chemical ecology
and the study of coevolution. Over the past decade, the pages of
New Phytologist have been publishing increasingly important
reviews (Strauss et al., 2005; Keeling & Bohlmann, 2006; Heil,
2008; Dudareva et al., 2013) and original studies (Leitner et al.,
2005; Agrawal et al., 2009; Huang et al., 2012; Zhang et al., 2013)
that have advanced our ecological and evolutionary understanding
of chemically-mediated interactions. In particular, classic questions
on the interactions of plants and herbivores, pollinators, and
microbes have been infused with modern chemical and molecular
methods, which has enhanced progress. In addition, there
continues to be a healthy tension between the use of model and
nonmodel study systems in chemical ecology, two ways to make
progress on interdisciplinary issues. The good news is that new
methods (e.g. genome-wide association mapping) can turn nearly
any organism into a ‘model’. As always, issues of chemical ecology
stand at the border between advancing knowledge of biodiversity
and basic plant biology with that of pest management and
maximizing plant production in the face of enemy attack (Fig. 1).
It was in this context that the 7th New Phytologist Workshop was
held in Ithaca, NY, USA early in the autumn of 2013. The
workshop, made up of over 30 participants (Fig. 2), was convened
by an organizing committee based at Cornell University, Ithaca,
NY, USA (Anurag Agrawal, Andre Kessler, Georg Jander, Robert
Raguso, Jennifer Thaler), spanning four departments (Ecology &
Evolutionary Biology, Plant Biology, Neurobiology and Behavior,
and Entomology). A committee of graduate students and
postdoctorates was also central to the planning and implementation of the workshop: Geoffrey Broadhead, Clare Casteel, M^onica
Kersch-Becker, Maya Lim, and Marjorie Weber. In addition to
funding from the New Phytologist Trust, further support came
from Cornell’s University Lectures Committee. In this paper I have
highlighted some of the meeting’s major emergent themes and
discussions.
Community and evolutionary ecology
Although it has long been recognized that the interaction ‘modules’
we study are embedded in a larger biotic and abiotic context, the
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field has been slow to embrace that larger context, especially in an
evolutionary sense. Yes, we have the classic papers and concepts
related to vegetational diversity impacting plant–herbivore interactions (Root, 1973), the concepts of diffuse coevolution (Strauss
et al., 2005), and advances in our understanding of geographic
variation in interactions within and between continents (Zangerl &
Berenbaum, 2003). However, admittedly, it is a challenge to
incorporate community complexity into our models. At the
workshop, Anurag Agrawal and Andre Kessler, and invited speakers
Erik Poelman (Wageningen University, the Netherlands) and Julia
Koricheva (Royal Holloway, University of London, UK) addressed
these issues in a variety of natural systems. Predicting the extent of
context dependence will always be a sticky issue, and this group
highlighted the importance of novel interactions between defense
and competition, plant biodiversity, and specificity in response to
the diverse assemblages of insects on plants (Poelman et al., 2011;
Milligan & Koricheva, 2013; Uesugi & Kessler, 2013). Perhaps the
biggest open gap is still identifying the most important (read: fitness
impacting) players in any given system; only after identifying these
important species can we make progress on evolutionary issues in a
community context.
‘Most species interactions involve at least three trophic
levels … and it behoves us to not only recognize this, but
to incorporate such interactions into our conceptual
models.’
The chemistry of attraction and defense
Following these lines, Scott Armbruster (Portsmouth University,
UK) presented a historical perspective on evolutionary transitions
between pollinator rewards and defense against herbivores
(Armbruster et al., 2009). Indeed, it was his classic work, and
through the continuing contributions of speakers Lynn Adler
(University of Massachusetts, Amherst, MA, USA) and Robert
Raguso that additional emphasis is being placed on the role of
chemistry in pollen, nectar, and floral volatile emissions (Raguso,
2009; Adler et al., 2012). Although we clearly have much to learn
and explore, it became apparent from the presentations that floral
chemistry is perhaps the most underappreciated aspect of pollination biology. Furthermore, not only are there important implications for pollinators, but also for the community of other plant
visitors. Given the complexity of interactions, we cannot assume
that floral traits are targeted at pollinators or herbivores; they may
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(a)
(c)
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(b)
(d)
Fig. 1 Chemical ecology and coevolution. (a,
b) A monarch butterfly caterpillar (Danaus
plexippus) taking bites of common milkweed
(Asclepias syriaca). After the exudation of
sticky toxic latex, the caterpillar wipes its
mouth clean. (c) A honey bee (Apis melifera)
approaching common milkweed flowers. (d)
Predation of a juvenile Colorado potato beetle
(Leptinotarsa decemlineata) by a stink bug
(Podisus maculiventris). All photographs
courtesy of Ellen Woods (University of
Connecticut, USA).
Fig. 2 Meeting participants at the 7th New
Phytologist Workshop (Taughannock Falls,
Ulysses, NY, USA).
Ó 2014 The Authors
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New Phytologist (2014) 202: 1122–1125
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have multiple roles, some of which are unexpected, and likely to be
context dependent (Huang et al., 2012).
Mechanisms of defense and counter-defense
The remarkable diversity of secondary compounds that have been
isolated from even a single species, for example, the diverse
glucosinolates from the model plant Arabidopsis thaliana, present
tremendous challenges for the study and interpretation of secondary metabolism. Does this compound diversity represent specific
adaptations targeted at different attackers, synergistic combinations of toxins, or some nonadaptive outcome (M€
uller et al., 2010;
Bekaert et al., 2012)? Genetically modified plants, network
analysis, and the dissection of hormonal pathways are all contributing to unravelling the physiological basis and evolutionary
underpinnings of secondary metabolism (Kliebenstein, 2012)
(with contributions from Georg Jander and invited speakers Dan
Kliebenstein, University of California, Davis, CA, USA and Martin
Heil, Cinvestav, Irapuato, Mexico). For defensive responses, there
are general mechanisms through which plants respond, and many
additional pathways for fine-tuning the specific plant response
(Heil et al., 2012). Finally, Noah Whiteman (University of
Arizona, Tucson, AZ, USA) spoke about the evolution of herbivory
in flies, and the role of adaptations in metabolism and detoxification that have facilitated shifts of drosophilids as leaf mining
herbivores of the Brassicaceae (Whiteman et al., 2012). Indeed, the
transition to herbivory (from saprophagy) appears to be dependent
both on the evolution of novel genes and the modification of
existing stress and toxin-detoxification genes. Although it is still
unclear how general these results are, studying the genetic basis and
evolution of plant feeding (and specialization to various plant parts)
could well be revolutionized in the coming decades.
(Poveda et al., 2012). Higher trophic level interactions, focusing on
predation risk, and its cascading effects on prey behavior and
physiology was the focus of presentations by Jennifer Thaler and
invited speaker Oswald Schmitz (Yale University, New Haven, CT,
USA). That predation risk alone can have major consequences not
only for prey behavior and plant damage, but also nutrient cycling,
highlights the dramatic extent to which pieces of ecological webs are
connected (Hawlena et al., 2012; Thaler et al., 2012). Most species
interactions involve at least three trophic levels, occur in a landscape
context, and change over ontogeny, and it behoves us to not only
recognize this, but to incorporate such interactions into our
conceptual models. Although tri-trophic theory is well-established,
we are still developing strong predictions for these other axes.
Conclusion and speculation
These are exciting times to be studying chemical ecology and
coevolution. Advances and availability of tools, techniques, and
information (i.e. genomes and phylogenies) are enhancing our
ability to address classic questions. The most influential emerging
work is integrative in some way, crossing boundaries or approaches
(i.e. looking at roots, including microbes, incorporating insect
physiology, etc.). If plant–animal interactions are truly a model for
how species interact more generally, then we can expect to see
substantial progress in understanding both mechanisms and
outcomes of such interactions in the coming decades.
Anurag A. Agrawal
Department of Ecology and Evolutionary Biology, Cornell
University, 425 Corson Hall, 215 Tower Road, Ithaca,
NY 14853, USA
(tel +1 607-254-4255; email [email protected])
Scaling up and out
If what happens in our Petri dishes, laboratories, or even local field
sites cannot be generalized to larger scales, then our science is in
trouble. Four speakers focused on different aspects of scaling in
plant–animal chemical ecology and coevolution. Thinking of
plants as dynamic organisms has been the rule within circles of
plant biologists for decades. Nonetheless, this is often not widely
acknowledged. Karina Boege (Universidad Nacional Autonoma de
Mexico, Mexico City, Mexico) addressed the generality of plant
phenotypes by considering changes that occur during plant
ontogeny. Indeed, ontogenetic switches in plant phenotypes bear
on many issues from simply the methods of measuring plant traits, to
constraints on the expression of phenotypes, to the evolution of
multiple integrated traits (Boege & Marquis, 2005). The intersection of developmental changes through a season and the order of
pest arrival (Viswanathan et al., 2007) generated interest and
discussion in terms of understanding how plants and insects can
dynamically shape the assemblage of insect communities. At the
other end of the spectrum, Katja Poveda (Cornell University, Ithaca,
NY, USA) focused on landscape ecology, and whether environmental heterogeneity at the landscape scale translated into predictable local trophic interactions that can impact plant productivity
New Phytologist (2014) 202: 1122–1125
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Ó 2014 The Authors
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Ó 2014 The Authors
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Key words: chemical ecology, coevolution, community ecology, defense,
interactions, plant–insect interactions.
New Phytologist (2014) 202: 1122–1125
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