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Complex factors determine where hawkmoths lay their eggs

Ecological interactions are often not simple or straightforward in nature. Instead, they commonly represent trade-offs between different processes so that the best compromise is reached in the end. This is exactly what scientists from the Max Planck Institute for Chemical Ecology found when they investigated the choices made by female tobacco hawkmoths (Manduca sexta) when laying their eggs.

The hawkmoths did not always make the obvious choice when placing their eggs on the leaves of plants that would provide food for the larvae, once they hatched. Previous research had shown that tobacco hawkmoths avoid laying their eggs on plants where they smell the feces of other hawkmoths. “This is apparently their way of avoiding food competition. Therefore, we wondered whether the moths also avoid plants infested by other herbivorous insects,” explained study first author Jin Zhang.

In the lab, the researchers gave female hawkmoths a choice between laying their eggs on sacred Datura plants (Datura wrightii) that were infested with three-lined potato beetles (Lema daturaphila) or Datura plants that had no potato beetles. Both adult and larval potato beetles feed on the leaves of this plant, and the researchers hypothesized that the hawkmoths would avoid plants where potato beetles were present in order to ensure the maximum supply of food for their offspring. 

But the hawkmoth females surprised the researchers by laying their eggs, preferentially, on the leaves of Datura plants that already hosted numerous potato 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,” explained study leader Markus Knaden.

“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.”

Tobacco hornworms, the larvae or caterpillars of tobacco hawkmoths, are heavily parasitized by the wasp Cotesia congregate, which lays its eggs in the caterpillars. Up to 90 percent of these caterpillars are parasitized by wasps and die shortly after the wasp larva hatches. Female hawkmoths therefore need to consider not only the available food supply for their larvae, but also their potential exposure to this parasitic wasp species.

The experts analyzed the odor given off by Datura plants when they carry an infestation of three-lined potato beetles compared to the odor emitted when there is no infestation. They found that infested plants produce more alpha-copaene in the in their odor when the beetles and their larvae are present. Interestingly, these three-lined potato beetles coat themselves with their own feces, possibly as a means of deterring would-be predators and parasites. 

The research team then tried to establish how exactly the tobacco hawkmoth females detect the presence of the molecular substance alpha-copaene. Of the 70 potential chemical receptors present in the hawkmoths, the researchers identified a single one, Or35, as the odorant receptor activated by alpha-copaene. They suggest that this receptor is probably involved in the moth’s choice of where to deposit its eggs.

Next, the experts tested the choices made by the wasps (Cotesia congregate) that parasitize tobacco hawkmoth caterpillars. They found that the wasps preferred the odor of plants on which tobacco hornworms were feeding, but they also avoided the odor of plants that were infested with potato beetles. These results were confirmed by assays in an experimental tent containing Datura plants infested by tobacco hawkmoths only, or by tobacco hawkmoths and potato beetles together. Wasps also avoided plants with beetles in this setting.

The findings indicate that female tobacco hawkmoths, when choosing where to lay their eggs, weigh up the benefit for their larvae of having no food competition against the disadvantage of being parasitized by the wasps. Although tobacco hornworms develop more slowly on plants that are additionally infested by beetles, 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 [their offspring] from predators,” concluded study co-author Bill Hansson.

The researchers will focus future studies on the reasons why Datura plants emit different odors depending on the insects that feed on them. They plan to use interdisciplinary approaches that also consider, for example, the role of microorganisms in these complex interactions, and hope to uncover further exciting aspects of the multifaceted interactions between living organisms.

The study is published in the journal Current Biology.

By Alison Bosman, Staff Writer

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