Few insect behaviors are more iconic than the proverbial moths circling the lamps at night.
Artist: Dave McKean
These observations are prime examples of the supposedly stereotypic
insect responses to external stimuli. In contrast, in our new publication "A Decision Underlies Phototaxis in an Insect", we describe experiments suggesting that insects
appear to make a value-based decision before approaching the light.
However, compared to us, an insect’s decisions can take very different
aspects into account. For instance, when a fruit fly (Drosophila)
decides whether to approach light, it takes its flying ability into
account. If any parameter of flight is sufficiently compromised, it is
better to hide in the shadows, whereas the full ability to fly emboldens
the animal to seek out the light. In a way, these results are
reminiscent of the confidence with which a certain cartoon bee
approaches a window:
Shifting the value of light
Perhaps the most beautiful result of this work is the first
investigation into the neurobiological mechanisms underlying the
different valuation of light (or dark) stimuli in flying and non-flying
flies. We found that the tendency of flies to approach or avoid light is
not an all-or-nothing decision, but that different fly strains and
different manipulations of flying ability show different degrees of
approach/avoidance as well as indifference. Experiments with transgenic
flies showed that we can push the flies’ preference back and forth along
this ‘photopreference’ gradient by activating or inhibiting neurons
that secrete either dopamine or octopamine, respectively. Octopamine and
Dopamine are so-called neuromodulators, known to be responsible for
valuation processes in other experiments across animals and in the case
of dopamine also humans. Commonly, they do this by modulating the
activity of neurons involved in processing sensory stimuli, such that
the value of these stimuli to the animal changes after the modulator is
applied.
In our case, activating dopamine neurons made flightless flies which
would otherwise avoid light, approach it. Activating octopamine neurons,
on the other hand, made normal flies, which approach light, hide in the
shadows, despite the manipulation leaving their flying capabilities
intact. The results obtained after inhibiting these neurons were mirror
symmetric: blocking dopamine neurons from firing made the flies seek
darkness without affecting their flying ability. Wingless flies with
their octopamine neurons blocked approached the light as if they could
fly. These results inspired the following illustration of how these
neuromodulators may cooperate to orchestrate the evolutionarily
advantageous decision for insects when faced with a light/dark choice:
Illustration
of the hypothetical balance between octopaminergic/tyraminargic (OA/TA)
and dopaminergic (DA) neurons establishing the valuation of light/dark
stimuli in fruit fly photopreference experiments.
Future research will show whether these same neurons indeed change their activity when the flying ability is manipulated, as one would expect from these results.
Ecological relevance
It is possible that the evolutionary origin and ultimate ethological
relevance may be found in the behavior of flies which have just emerged
from their pupal case. The wings of these young adults are still folded
up as the insect first needs to pump blood into the veins of the wings
to expand them. During this time, the flies perch underneath horizontal
surfaces and avoid light. Even when the wings are fully expanded, but
not capable of supporting flight just yet, this behavior persists. Only
once the wings are ready for flight, do the flies perch on top of
horizontal surfaces and approach light.
Source: hawaiireedlab.com
Adult flies in the wild that live on rotting fruit probably face the
challenge of the sugary liquid of the fruit occasionally gumming up
their wings, only for the next rain to wash them clean again. We
mimicked this situation in one of our experiments by gluing the wings
together with sucrose solution and subsequently removing the sugar glue
from the flies’ wings with water. As expected, the flies approached the
light before the treatment, avoided it when the wings were unusable and
approached it again after the ‘shower’.
Sparse literature
The first mention in the literature of adult flies with compromised wings being less attracted by light was by Robert McEwen in 1918.
In the intervening 49 years, we could not find any mention of this
phenomenon in the scholarly literature. Only in 1967, one of the
founding fathers of Drosophila neurogenetics, Seymour Benzer, published work mentioning adult flies with deformed wings being less phototactic, but
without any insight into the underlying neurobiology. It took yet
another 49 years after Benzer’s work without any mention in the
literature, before the first neurobiological components of this case of
insect behavioral flexibility were published, 98 years after the
original discoverer McEwen. Our postdoc, E. Axel Gorostiza, the first
author of the paper, will start his own laboratory on this topic, so it
seems unlikely that it will take yet another 49 years for the next
publication to appear.
Reproducibility - Open Science
Of course, all our raw data are available from figshare. This was also the first paper from our laboratory where all authors were listed with their ORCID IDs and all materials and protocols were referenced with their RRIDs and protocols.io DOIs, respectively. All previous versions of the article are available as biorxiv preprints as well.
Freie Universität Berlin, Universität Regensburg, Germany.
Abstract:
Like a moth into the flame – Phototaxis is an iconic example for
innate preferences. Such preferences likely reflect evolutionary
adaptations to predictable situations and have traditionally been
conceptualized as hard-wired stimulus-response links. Perhaps therefore,
the century-old discovery of flexibility in Drosophila phototaxis
has received little attention. Here we report that across several
different behavioral tests, light/dark preference tested in walking is
dependent on various aspects of flight. If we temporarily compromise
flying ability, walking photopreference reverses concomitantly. Neuronal
activity in circuits expressing dopamine and octopamine, respectively,
plays a differential role in photopreference, suggesting a potential
involvement of these biogenic amines in this case of behavioral
flexibility. We conclude that flies monitor their ability to fly, and
that flying ability exerts a fundamental effect on action selection in Drosophila.
This work suggests that even behaviors which appear simple and
hard-wired comprise a value-driven decision-making stage, negotiating
the external situation with the animal’s internal state, before an
action is selected.
