Unexpected benefits from food competitors
When laying their eggs, female hawkmoths rather share a host plant with competitors in order to escape from parasitic wasps

Date:
January 10, 2022
Source:
Max Planck Institute for Chemical Ecology
Summary:
A research team has found that gravid tobacco hawkmoths (Manduca
sexta) show an unusual preference for Datura plants that are
already infested with leaf beetles when laying their eggs. The
beetles and their larvae actually compete with tobacco hornworms,
the larvae of Manduca, for food.

Plants infested by beetles change their odor profile and increase
the production of the substance alpha-copaene, making them, however,
more attractive to tobacco hawkmoths. Despite food competition,
tobacco hornworms seem to benefit from their mothers' choice of such
host plants because in the presence of beetles and their larvae they
are better protected from parasitic wasps that avoid beetle-infested
plants. The researchers were also able to identify the tobacco
hawkmoths' olfactory receptor that controls this behavior.



FULL STORY ==========================================================================
By choosing the best possible oviposition site, many insects set the
course for the best possible development of their offspring: There
should be enough food available and the larvae that hatch from the
eggs should be as safe as possible from pathogens and predators. In an
earlier study, the research team led by Markus Knaden and Bill Hansson
from the Department of Evolutionary Neuroethology had already been able
to demonstrate that tobacco hawkmoths avoid laying their eggs on plants
where they smell the feces of their conspecifics.

"This is apparently their way of avoiding food competition. Therefore,
we wondered whether the moths also avoid plants infested by other
herbivorous insects," first author Jin Zhang summarizes the question of
the current study.


========================================================================== However, behavioral experiments with sacred datura (Datura wrightii),
which were infested by the three-lined potato beetle Lema daturaphila,
resulted in an unexpected surprise: Quite obviously, female tobacco
hawkmoths even preferentially laid their eggs on these Datura plants,
compared to plants that were not infested by the beetles.

"To be honest, we were a little frustrated at first because we had
expected the experiments to confirm our initial hypothesis, namely
that egg-laying tobacco hawkmoths avoid food competitors. In our case,
however, the unexpected observation suddenly made sense when we realized
that beetle-infested plants smell quite differently and that parasitoid
wasps, which often use plant odors to find their host insects, are less efficient at detecting tobacco hornworms on beetle-infested plants,"
explains study leader Markus Knaden.

In nature, it is not always possible to avoid all dangers and at the
same time select a place with abundant food. For example, studies suggest
that up to 90% of Manduca sextacaterpillars are parasitized by the wasp
Cotesia congregata.

This parasitoid wasp lays its eggs in the caterpillars and transmits
pathogens.

Parasitized tobacco hornworms usually die, when the wasps' offspring
hatches.

The researchers used this knowledge to study the seemingly strange
behavior of the tobacco hawkmoths in more detail. They analyzed the odor
Datura plants emit when they are infested by three-lined potato beetles
and compared it with control plants without infestation. And, finally,
they noticed an unusual increase of the substance alpha-copaene in the
plants' odor bouquet.

How the moths detect and process this odor was the next question the
team answered. Since tobacco hawkmoths have about 70 odorant receptors
that would be potential candidates for detecting alpha-copaene, it would
have been very time- consuming to test them all individually. Instead,
a combination of complex molecular methods allowed the scientists to
reduce the number of candidates from about 70 to 6, and finally identify
Or35 as the odorant receptor activated by alpha-copaene and probably
involved in oviposition.

The researchers also examined the odor-guided behavior of the parasitoid
wasps.

Choice experiments in which the wasps could choose between two odors
revealed, on the one hand, that Cotesia congregata wasps preferred
the odor of plants on which tobacco hawkworms were feeding to control
plants. On the other hand, these behavioral assays also demonstrated
that the wasps avoided the odor of plants that were infested by Lema daturaphila beetles. These results were confirmed by assays in an
experimental tent containing Datura plants infested only by tobacco
hawkmoths or by tobacco hawkmoths and beetles. Wasps also avoided plants
with beetles in this setting.

Although the development of tobacco hornworms on plants that are
additionally infested by beetles is impaired in comparison to the
development of caterpillars on non-infested plants, the mother moths
accept this disadvantage when laying their eggs. The advantage of
protecting their offspring from parasitic wasps must therefore outweigh
the disadvantage of food competition.

Such cost-benefit trade-offs play a significant role in many ecological interactions. "Our results show that in nature, simple explanations are
often not sufficient. Tobacco hawkmoths do not only have to take into
account, whether a plant is a good food substrate for their offspring,
but also whether potential competitors are already present, and whether
the presence of these competitors could even help to hide from predators,"
Bill Hansson summarizes the results.

Why Datura plants emit different odor depending on the insects that
feed on them will be addressed in further studies. Both Manduca
sexta caterpillars and the larvae of the three-lined potato beetle
Lema daturaphila are chewing insects and cause similar damage to plant
tissue. Presumably, microorganisms in the oral secretions of the animals
play a role. Interdisciplinary approaches that also focus, for example,
on the role of microorganisms in these complex interactions may help
to uncover further exciting aspects of the multifaceted interactions
between living organisms.

========================================================================== Story Source: Materials provided by
Max_Planck_Institute_for_Chemical_Ecology. Note: Content may be edited
for style and length.


========================================================================== Journal Reference:
1. Jin Zhang, Syed Ali Komail Raza, Zhiqiang Wei, Ian W. Keesey,
Anna L.

Parker, Felix Feistel, Jingyuan Chen, Sina Cassau, Richard
A. Fandino, Ewald Grosse-Wilde, Shuanglin Dong, Joel Kingsolver,
Jonathan Gershenzon, Markus Knaden, Bill S. Hansson. Competing
beetles attract egg laying in a hawkmoth. Current Biology, 2022;
DOI: 10.1016/j.cub.2021.12.021 ==========================================================================

Link to news story: https://www.sciencedaily.com/releases/2022/01/220110114143.htm
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