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Phototactic personality in fruit flies

first page of the fly phototactic personality paper
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a group of flies moving toward a light source, with a single fly moving in the opposite direction

Do animals as simple as flies have personalities?

Definitions of personality vary substantially across fields, and are often left implied. The heart of the phenomenon seems to be that individual organisms display idiosyncratic behavioral patterns that persist for a substantial amounts of time. By this definition, flies have abundant personality. The culmination of a couple years of work by Jamey Kain in our lab, our paper on fly personality was just published at PNAS.

The detection of such personality requires a method to statistically distinguish variability within the behavior of an individual from variability between individuals. If there is more variability between individuals than within (i.e. the observed behavioral distribution is over-dispersed compared to what would be expected from sampling error alone) – and the particular behavioral tendencies of individuals persist on subsequent re-evaluation then you have uncovered personality. There is mounting evidence in organisms ranging from pea aphids to trout exhibit personality in a wide variety of behaviors. We suspect that personality may be universal.

We came to work on this project while trying to map genetic differences between lab strains of Drosophila simulans that exhibit different light preferences. One runs toward light, while the other runs away from light, when startled. These strains are essentially isogenic, harboring no genetic diversity between individuals, and yet we found that the distribution of behavioral scores within each strain was broader than we’d expect based on sampling error alone (we gave each fly a choice to go toward or away from light 20 times, and thus had a fairly precise estimate of its preference).

This heterogeneity meant that mapping the genetic underpinnings of the difference in strain mean preference was going to require bigger sample sizes, and consequently be very labor intensive. That’s when we decided to build FlyVac, a platform for the autonomous manipulation of flies to measure phototaxis. That’s also when we realized that fly phototactic idiosyncrasy was an interesting phenomenon on its own.

So, after a couple years’ work, what have we learned about fly phototactic idiosyncrasy? A number of things:

    • All fly strains seem to have it. Only when we put blind flies into the device, or gave them symmetrical light stimuli did we observe behavioral distributions matching what we’d expect based on sampling error alone. In fact, the phenomenon is not limited to flies. The white clover weevil Ischnopterapion virens performed very similarly.
    • It is persistent. Flies recovered from FlyVac and tested up to 28 days later show significantly correlated phototactic preferences
    • Genetic differences between animals cannot explain their behavioral differences. There isn’t much genetic diversity to begin with in most of the lines we examined, but additionally we inbred them for 10 generations, mating daughters back to fathers or grandfathers (sorry flies). This did not reduce the magnitude of personality; if anything, it amplified it.
    • Personalities cannot be inherited (even by non-genetic means, such as epigenetics). Mating two flies with strong positive (or negative) light preferences had no effect on the behavioral distribution of their progeny. In all cases the progeny had behaviors identically distributed as the parents.
    • The gene white, and the neurotransmitter serotonin (whose synthesis may depend on white) act in wild type flies to suppress personality, driving behavior toward homogeneity.

Please see our paper for all the gory details:
Image of the title and authors of the FlyVac Paper

Why does non-heritable personality exist?

This will be the focus of forthcoming paper from our lab (hopefully soon). But there are two basic ideas. Personality could be essentially noise, i.e. non-adaptive, but tolerated for some other greater good. Possible greater goods include rapid development, or avoiding the metabolic costs of additional signaling pathways or neurons that would suppress the developmental stochasticity that generates the variability.

Alternatively, it might be inherently advantageous. Retaining a population with high diversity might mean that when a transient selective pressure arises that favors a subset of animals, they will successfully produce a subsequent generation. If that selective pressure goes away, then the non-heritability of the behaviors means that the subsequent generation will revert to the original (well adapted for typical conditions) distribution of behaviors immediately. Another consideration is that if behaviors are entirely predictable, they can be exploited. If flies always run toward the light, predators will learn this, and any fly that runs away from the light will have an advantage. This is an example of frequency-dependent selection, in which the fitness of a particular phenotype depends on the number of other individuals exhibiting it. Such dynamics often equilibrate to what economists and game-theorists call mixed strategies, when the optimal strategy entails acting randomly from instance to instance.

Jamey and I have a Q and A conversation about this work in the following video/podcast. If you stick around to the end of the video, we’ll take you on a walking tour of the lab, and show you FlyVac in operation:

Still frame from movie about FlyVac with Jamey gesturing

3 Responses to “Phototactic personality in fruit flies”

  1. John Charles Brown says:

    In the current hot summer I have been killing a lot of flies. A particularly difficult target was a very small green bottle. One technique I use is to chase the fly around with a vacuum cleaner hose. Hopefully the fly will aggressively react to the end of the hose, and get sucked into it. When this does not happen, and I remain persistent, the fly eventually tires (I guess the mitochondria in its flight muscles get depleted) and it settles on a surface, after which it is easy to get it into the vacuum cleaner.
    But the tiny green bottles are so light and have such strong muscles, that they always dodge away from the vacuum without engaging with it. That caused me to chase them for maybe 5 minutes, during which they had lots of interractions with the hose. This happened in particular with a pair which I had interrupted in the course of mating, which made them very persistent in getting back together as soon as possible. The next time they tried to mate, maybe half an hour later, I turned on the vacuum cleaner, and they immediately flew off in differing directions. I had conditioned them to associate the sound of the motor with the action at the end of the hose.
    This was pretty quick learning.
    I have also had a maggot problem, where flies have laid eggs in my vegetable waste, particularly when I cleaned out my old freezer. I noticed one maggot on the sink, and one that had climbed out of my waste bin and dropped to the floor. Little did I know that they were in their “wandering stage” where they go off and look for somewhere to pupate. In place of burrowing into the soil, they went under the edges of my rugs. A couple of weeks later, in really hot weather, they started hatching and I was vacuuming up around 30 flies a day. I eventually vacuumed up all the pupae and things got quiet about 5 days later.
    The flies bred in my house were much less active and aggressive than those coming in from the fields. It was really easy to vacuum them up. I suppose that they had very small muscles, given the restricted diet of their maggots.
    So flies reflect “nuture” from their larval stages, and we can condition flies. I wonder if maggots are also conditioned. Some fruit-fly maggots may associate light with a high glucose level, depending on where they were hatched within their food source.
    That would explain the variation in the personality of flies. The evolutionary advantage is that a fly could have a more frequent chance of finding food if it looked in the same sorts of places in which its larval form grew up. For example, fallen fruit at a particular time of year could be associated with lower light levels, than fruit still on the tree, slightly earlier in the year. In carcass-dwelling maggots, large carcasses would provide lower light levels than smaller ones. So, for example, if the crows kill off frogs they catch in the act of mating, due to recent rain, the maggots will be fonder of the light than those found in large animals that die in a drought.

  2. Administrator says:

    Hello John – thanks for the great comment. You’re absolutely right that flies are good learners. I remember reading that there are something like 50 published paradigms for training Drosophila. This review article does a good job of describing several of them major ones: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2814444/

    I think the kind of environmental and developmental experiences you’re describing could certainly contribute to the diversity of behaviors in wild populations of flies. But effects like these are unlike to explain the behavioral differences we saw in our experiments because all of those flies are reared on identical food, in identical light conditions. We even did an experiment where we also assured that all flies (and their parents) had identical social experiences. If the very slight environmental differences experienced by these flies accounts for their behavioral differences, the behavioral response must be phenomenally sensitive.

  3. John Charles Brown says:

    Thanks for the reply, and the data on fruit fly learning. I do Artificial Intelligence programming, in particular text analysis using NLP, machine-learning, and the sort of theory that Pinker writes about. So I am constantly intrigued by how much insects do with limited neural capacity. A few years ago people in the AI field were fascinated by ants allegedly giving each other directions to food by a long sequence of antennae movements. Dead reckoning in desert ants has also featured in a recent neuroscience book, Gallistel and King, “Memory and the Computational Brain”, although I find the arguments rather unconvincing.
    I have 3 personal experiences that I can’t forget.
    1) Watching leaf cutter ants in the museum, walking from the nest along a branch to the leaves, and returning with a cut leaf. One ant dropped the leaf, but clearly lacked the sequences to react to this, and returned to the nest, where it presented its non-existent leaf to a number of workers who appeared to select just the right sort of leaf for their particular purposes. It waited patiently for its “leaf” to be taken, but my patience ran out after 15 minutes. I suppose it would have re-set all its sequences when dark fell.
    2) A dragon fly was cruising over the water, bobbing up and down as it captured flies. I saw it missed one fly, and it then flew back along its path, this time putting the fly on its other side. I suppose this behaviour maximised capture in the face of wind or asymmetry in muscles etc., in prey or predator.
    3) I sat down in front of a low wall in a garden. I was wearing a light-brown jacket with dark brown leather trimmings. A bee landed on me and appeared to apply its mouth-parts to the leather trimmings. Then a second one did the same thing. When I looked at the wall, about 4 feet behind me, I could see that it was similarly coloured to my jacket, and had patches of lichen of fairly similar colour to the leather trimmings. A number of bees were visiting the lichen. I still think about that a lot. The bees must have suppressed taste and smell signals and distance-from-hive, and perception of height, allowing colour to dominate. Even then, the colours were only approximately correct. I wonder too why they were not attracted to fly closer to the other bees. Maybe these were symptoms of the “empty-hive” disorder?

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November 15, 2012 on 3:16 am    ~    3 Comments