Ovipositing insects use odor cues to select suitable food substrates for their offspring in order to increase the survival rates of the larvae. Scientists from the Max Planck Institute for Chemical Ecology demonstrated that not only may plant odors determine the best oviposition site, but also the frass of other larvae of the same species. They specified the repelling substance in the feces of tobacco hornworm larvae which signals the presence of competing conspecifics to the female moths. Moreover, the researchers were able to identify an odorant receptor which is involved in the detection of the typical smell of larval frass and thereby governs competition avoidance during oviposition (Proceedings of the National Academy of Sciences of the United States of America, October 2019, DOI: 10.1073/pnas.1913485116 PNAS).
Very hungry caterpillars
Tobacco hornworms (Manduca sexta) are extremely voracious. Their Latin name Manduca is derived from the verb manducare,
which means eating or chewing. These insatiable caterpillars, which may
become as big as an adult’s finger, do not do anything but eat and chew
all day long. Therefore, a single larva is able to defoliate a host
plant, such as the wild tobacco Nicotiana attenuata or sacred datura Datura wrightii (at least small plants) completely. Hence, one plant is seldom enough to feed a second caterpillar.
“We
knew already that moths select their oviposition sites carefully. So
far we and others basically focused on the idea that the moths detect
changes in the odor profiles of plants that have already been attacked
by caterpillars and therefore lay their eggs somewhere else. We were
interested in whether moths also consider information that is provided
by the larvae, i.e. by the potential competitors of the moths’
offspring, directly,” explains Markus Knaden, one of the main authors of
the publication.
It seemed plausible that tobacco hawkmoths
would try to avoid competition for their offspring. Nevertheless, that
one specific class of volatile compounds in the larval feces (6-carbon
aliphatic acids) would be sufficient to trigger avoidance behavior came
as a surprise. Behavioral assays in the wind tunnel in which moths were
exposed to individual odor components on filter paper clearly showed
that moths were repelled by some of the frass-related compounds.
In ovipositing moths, the receptor IR8a regulates the avoidance of larval frass
This
specificity in the avoidance response to 6-carbon aliphatic acids
allowed the scientists to elucidate the molecular basis of the behavior.
By using the novel technique CRISPR/Cas9, they knocked out specific
receptor proteins in the antennae, the moth’s nose, that were crucial
for the detection of these compounds, and were thus able to show that
the ionotropic receptor 8a (IR8a) governs the avoidance response to
larval feces.
“Surprisingly, so far no one has investigated how
moths detect signals from larval frass. Our experiments with moths which
lacked IR8a proteins demonstrated that without these proteins,
ovipositing moths were unable to detect and avoid conspecific
competitors and laid their eggs at places where the chances for their
offspring were diminished. Our study shows for the first time that the
IR8a pathway is essential for mediating acid avoidance caused by
caterpillar feces,” summarizes Jin Zhang from China, who is first author
of the study and whose research project at the Max Planck Institute for
Chemical Ecology was supported by the Alexander von Humboldt
Foundation.
Evolutionary context and perspective
Plant-insect
interactions are diverse and highly complex. They have evolved over the
course of evolution and can be adapted whenever a parameter changes. It
is not a new discovery that tobacco hawkmoths lay significantly fewer
eggs on plants that are already being attacked by caterpillars. In
addition, the smell of larval feces is known to attract predators, the
enemies of the larvae. However, it was not known that the same larval
frass ensures that conspecifics which would otherwise compete for food
are kept at a distance. Thus, the chemical signal from the frass helps
not only the caterpillars which are already feeding on a plant but also
the hovering moths: By avoiding the smell of larval feces, they may find
better food for their offspring.
The recently developed genetic tools provide new opportunities to study odor-guided behavior in Manduca sexta
and other pest insects in more detail. Researchers are particularly
interested in addressing the following questions: Which factors, such as
flower scents, humidity and CO2, guide insects to their host plants?
Which receptor proteins regulate responses to specific odors? What genes
are involved in these particular behaviors?
Fundamental
knowledge gained from these studies may help to better prepare us for
the agricultural challenges resulting from climate change. [AO/KG]
Original Publication:
Zhang,
J., Bisch-Knaden, S., Fandino, R. A., Yan, S., Obiero, G. F.,
Grosse-Wilde, E., Hansson, B. S., Knaden, M. (2019). The olfactory
co-receptor IR8a governs larval feces-mediated competition avoidance in a
hawkmoth. Proceedings of the National Academy of Sciences of the United
States of America, DOI: 10.1073/pnas.1913485116
https://doi.org/10.1073/pnas.1913485116