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Fruit Fly Eyes and More Surprises for Darwin

Photo: Drosophila melanogaster, by Sanjay Acharya, CC BY-SA 4.0 , via Wikimedia Commons.

Those tiny, pesky fruit flies have gotten no respect. Sprayed, swatted, and irradiated, the little flying machines have been treated by humans as better off dead. Hermann J. Muller got a 1946 Nobel Prize for blasting Drosophila melanogaster fruit flies with X-rays, finding that the barrage gave them lethal mutations. Scientists have manipulated their genes to make them grow legs out of their antennae or grow four wings, rendering them helpless. And worried farmers have convinced politicians to spray malathion over cities like Los Angeles to prevent invasions of fruit flies. But before killing off all these critters, it would be worth taking a closer look at their design.

Eyes’ Size

An adult fruit fly emerges from the egg and pupa in about two weeks. As the eyes are developing in a fruit fly embryo, an amazing process unfolds. A wave of signals sweeps across stem cells in the budding compound eye, switching on certain progenitor cells to stop proliferating and become unit eyes (ommatidia) and signaling others to undergo programmed cell death (apoptosis). The result is an “organ of extreme perfection” to call on Darwin’s phrase that is not only geometrically beautiful but functional for the fly — and it comes in matching left and right sides, like a pair of rubies.

Navarro et al. published a paper about how this works in PLOS Biology. In the same journal, Marco Milán from the Barcelona Institute of Science and Technology summarized the paper, explaining how the regulated process achieves “size precision” as the eye grows. Internal controls reduce “fluctuating asymmetry” (FA), a wobbly mismatch of size and shape. In effect, the growing cells of the eye do The Wave.

A new study unravels an organ-intrinsic mechanism of growth control in the developing fly eye that confers size precision through feedback interactions between proliferating and differentiating cells. This mechanismreduces eye size variability between and within animals, thus contributing to the symmetry between contralateral eyes and having a clear potential impact on eye functionality. In the growing eye primordium, a wave of differentiation moves anteriorly, whereby proliferative progenitors located anterior to the wave are recruited as differentiating retinal cells that exit the cell cycle (Fig 1). When the wave reaches the anterior-most region of the primordium, no remaining progenitors remain in the tissue, and the final eye size is attained. The movement of the differentiation wave relies on the activity of 2 morphogens [shape generators], the BMP homolog Dpp and Hedgehog (Hh), which are produced by differentiating retinal cells that signal anteriorly to nearby proliferating cells to recruit them as new differentiating retinal cells. [Emphasis added.]

The Barcelona team calls this “feedback control of organ size precision mediated by BMP2-regulated apoptosis.” The result is a geometrically perfect oval-shaped eye with 800 ommatidia neatly arranged like hexagonal cells on a curved honeycomb. The curved shape gives the fly greater than 180-degree visibility on each side. 

Much more must be going on, because bristles grow between each ommatidium to provide touch sensation for the fly, and each unit must be wired properly to the optic nerves going to the developing brain. What’s more, the two eyes must become exact mirror images of each other to prevent fluctuating asymmetry so that the fly can navigate with precision. The authors believe a similar process controls wing development so that the wings match. Imagine a pilot trying to maneuver a plane with one wing shorter than the other!

This one example illustrates an astonishing amount of control in an insect just a few millimeters in length. And they only investigated this in one organ — the visual system — while all the other body systems are also in the process of developing simultaneously: circulation, digestion, reproduction, muscular, flight, sensory, jointed appendages, and much more.

The authors, Navarro et al., make a logical mistake in how these controls came about:

Three features should have resulted in a strong evolutionary pressure to maximize the precision in eye size: First, size impacts vision directly, as image resolution and contrast sensitivity is proportional to the number of light sensing units in the eye; second, making and maintaining the eyes is energetically very expensive, so there is a pressure to match eye size to vision needs; and third, left and right eyes must survey a symmetrical part of the space, so eye asymmetry, which could be driven by developmental noise, should be minimized.

An unguided, blind process could not care about what “should” be done and is incapable of being pressured to do anything. Stephen Crane once quipped, “A man said to the universe: ‘Sir, I exist!’ ‘However,’ replied the universe, ‘The fact has not created in me a sense of obligation.’” Much less could molecules know about or care about “evolutionary pressure.” The authors are admittedly surprised how all these parts come together so neatly:

Biological processes are intrinsically noisy, and yet, the result of development — like the species-specific size and shape of organs — is usually remarkably precise. This precision suggests the existence of mechanisms of feedback control that ensure that deviations from a target size are minimized.

Right Flight

Here’s another fruit fly trick from recent news. How did the fruit fly make a sharp turn? This is not a joke. Sharp turns don’t just happen in a fruit fly because it has wings. They are controlled by specialized neurons. 

This month, Ros et al. published their findings in Current Biology about “Descending control and regulation of spontaneous flight turns in Drosophila.” In the same issue, Matthieu Lewis summarized the research about how and why fruit flies make sudden zigs and zags while flying.

Upon detecting an attractive odor plume, a fly surges upwind, followed by crosswind casting separated by counterturns when the plume is lost. While the sensory control of turning and casting is shared across most animals, little is known about its neural underpinnings. In a paper in this issue of Current Biology, Ros et al. report the identification and functional characterization of a pair of bistable descending neurons that orchestrate casting during flight behavior in the fly Drosophila.

These neurons, Ros et al. explain, consist of “couplets of one excitatory and one inhibitory descending cell form functional units.” As with many systems in biology and in engineering, an accelerator is paired with a brake, providing fine control with a push-and-pull combination of systems responsive to input from the surroundings. Particular “command units” of descending neurons enable a fruit fly to make sharp turns called saccades. “An array of excitatory and inhibitory neurons provides input to the saccade network,” the authors say about one of their major findings.

Within the central nervous system of insects, descending neurons (DNs) constitute a critical stage in the transformation of sensory input in the brain into motor commands in the ventral nerve cord (VNC). Drosophila possess ∼650 pairs of DNs, some of which appear to function as specialized command neurons for specific behaviors, including courtship, walking backward, turning, take-off, and landing. Thus, DNs provide a logical starting point for investigating the circuits that generate and regulate flight saccades.

Stop for a moment to picture this little millimeter-range creature containing 650 pairs of descending neurons each programmed for specific commands. One fires, and the fly walks backward. Another fires, and the fly comes in for a landing. Another fires, and boy fly courts girl fly. This sounds much more astonishing than a computer-controlled robotic drone. 

By ablating one or the other of the descending neurons (DNs) involved in saccades, the team supported their hypothesis that the couplet functions as a saccade-generating unit (SGU). 

The altered saccade dynamics and temporal distribution after ablation support the hypothesis that each DN can produce saccades independently of the other but with different dynamics than those of control flies. The results support a working hypothesis that the two DNs play complementary roles by activating different components of the motor circuit in the VNC responsible for generating saccades. Together, functional imaging, unilateral activation, and ablation experiments suggest that two pairs of descending interneurons, DNae014 and DNb01, function together as saccade-generating units (SGUs) to execute commands for spontaneous turns during flight.

Louis gives examples in other animals, from insects to mammals, that use a similar “sector search” strategy during navigation. But why would a fruit fly need to make a sharp turn?

Saccades are thought to benefit flying animals in several ways. From a sensory perspective, saccades may restrict the deleterious effects of motion blur to brief moments interjected within longer sequences of gaze stabilization. Brief bursts of saccades in the same direction may aid local search strategy by allowing the animal to quickly scan the local environment for salient visual and olfactory features. More recently, it has been suggested that comparing sensory measurements immediately before and after each saccade might enable flies to estimate key parameters that are otherwise not directly measurable, such as the direction and magnitude of the ambient wind. For all these hypotheses, the timing between saccades is critical

Critical timing, fine control, and convergent strategies between unrelated animals — such concepts defy Darwin’s bluffing notion of the creative power of natural selection. At one point, the authors acknowledge that this looks like engineering.

The activity levels between the left and right DNae014 cells followed an inverse, highly non-linear relationship, analogous to “flip-flop” components in digital electronic circuits (Figure 1J) and reminiscent of neurons identified in the steering behavior of male silkmoths. Further, the DNb01 cells synapse directly onto contralateral DNae014 cells. This is a simple reciprocal inhibitory motif, consistent with a network responsible for binary turning to either the left or the right.

More to Come

We’re not done with design in fruit flies. Next time, we will look at some of the sensory apparatus within these little insects. While fruit flies are convenient lab animals for study, undoubtedly similar systems can be found in even smaller flying insects like mosquitoes and gnats, all of which, being heavier than air, “evolved” powered flight and all their related systems because of “selection pressure.” Not.