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Hear This: Cricket Ears Evolved Like Vertebrate Ears

Evolution News
Photo: A katydid, by Evolution News.

As in Jeopardy, here is the answer before the question. 

Despite the insect ear’s tiny dimensions, its mode of operation strikingly resembled that of vertebrate ears. Apparently, evolution has provided similar solutions to the spectral processing of sounds.

The question is: “How did crickets get finely tuned hearing organs?” In Evolution Jeopardy, winners know the secret to winning big: give credit to evolution.

The quote is from a paper by Vavakou et al. in PNAS, “Tuned vibration modes in a miniature hearing organ: Insights from the bushcricket.” Here is the context:

Most hearing organs contain an array of sensory cells that act as miniature microphones, each tuned to its own frequency like piano strings. Acoustically communicating insects like bushcrickets have evolved miniscule hearing organs, typically smaller than 1 mm, in their forelegs. It is still unknown how the sensory structures inside the leg vibrate in response to sound. Using advanced imaging techniques, we meticulously mapped the nanovibrations in the bushcricket ear. We discovered a complex motion pattern in which structures separated by only 1/50 mm showed systematic tuning differences. Despite the insect ear’s tiny dimensions, its mode of operation strikingly resembled that of vertebrate ears. Apparently, evolution has provided similar solutions to the spectral processing of sounds. [Emphasis added.]

Having paids the obligatory homage to Darwin, the four authors from the Netherlands and Germany get down to the science. 

The Findings

Bushcrickets, also known as katydids, are those green grasshopper-like insects that fascinate children because of their leaf-like camouflage. Using Optical Coherence Tomography (OCT), the European team obtained detailed images of the hearing organs of bushcrickets. The hearing organ on these orthopterans are located on the tibia just below the knee. Called the crista acoustica (CA), this organ, only 0.9 mm long, contains a series of sensory dendrites of decreasing length from the proximal to distal ends of the CA, oriented perpendicular to it. They look like piano strings, and presumably perform a similar function to the hair cells in the Organ of Corti of the mammalian cochlea. The ventral ends of the dendrites in the CA are embedded in the distal wall (DW), analogous to the basilar membrane in the cochlea. The dorsal ends of the dendrites are connected to cap cells which resemble the hair cells in vertebrate cochleae, where acoustic transduction to electric (neural) signals take place. 

Striking Similarities

Other than location (in the heads of vertebrates and on the legs of insects), the functional similarities of the CA to the mammalian cochlea are striking, except that the cochlea is 40 times as long as the insect hearing organ! It’s a remarkable example of convergence already, and there is more to come.

Over the entire length of the CA, we were able to separate and compare vibrations of the top (cap cells) and base (dorsal wall) of the sensory tissue. The tuning of these two structures, only 15 to 60 μm (micrometer) apart, differed systematically in sharpness and best frequency, revealing a tuned periodic deformation of the CA. The relative motion of the two structures, a potential drive of transductiondemonstrated sharper tuning than either of them. The micromechanical complexity indicates that the bushcricket ear invokes multiple degrees of freedom to achieve frequency separation with a limited number of sensory cells

Here is a case of fine-tuning at a micromechanical level in the acoustical response of the bushcricket hearing organ. The CA lies between two tympanic membranes, analogous to eardrums in vertebrates. The dorsal and ventral tympana vibrate in phase, moving synchronously, and appear to move in and out by a double hinge. The membranes tend to squeeze the CA, setting up waves that make the DW (dorsal wall) and the CC (cap cells) vibrate in different ways.

In summary, we recorded sound-induced vibrations in the bushcricket hearing organ using OCT vibrometry. The depth resolution of this technique yielded an unprecedented set of measurements. First, we measured the sound-induced motion of the anterior tympanum and the posterior tympanum at the same time. Our measurements confirmed that the two tympana bulged in and out simultaneously (Fig. 2E). Second, the septum between them followed the motion of the posterior tympanum (Fig. 2B). Third, we made a detailed and quantitative comparison between the sound-induced vibrations of the DW and the CC. The responses of both structures were tuned (Fig. 3), and there exist systematic differences between them in their tuning across the whole length of the sensory organ (Fig. 4). The differential motion of these structures was more sharply tuned than the absolute motion of either of them (Fig. 5 and SI Appendix, Fig. S2).

What this means is that two different acoustic responses sharpen each other. In the DW, which is stiffer along its length, and cap cells, which are each more sensitive, responses cooperate to improve the tuning response of each sensory dendrite. The fact that both weak responses are out of phase reinforces the tuning precision of the organ as a whole. Figure 6E in the paper shows a graph of improved resolution when the vector difference between them is graphed. It’s a clever way to get more resolution out of the tiny pressure waves that impinge on the hearing organ.

Impedance Matching

Another similarity to the vertebrate ear is found in the impedance matching. In our ears, the eardrum gathers the pressure waves of sound over a large surface, and through the lever action of the ossicles, transmits it through a smaller surface (the stapes) to the oval window of the fluid-filled cochlea. This amplifies the signal for the hair cells lining the Organ of Corti. The bushcricket has impedance matching, too:

Intriguingly, the double-hinged motion (Fig. 2) shows a striking resemblance with the coupling of sound into vertebrate inner ears, where a lever system (middle ear ossicles) converts the larger motion of a larger surface (eardrum) to smaller motions of a smaller area (stapes). In vertebrate ears, this configuration provides an impedance match between airborne sound and the vibrations in the fluid-filled inner ear. The hinged motion of the bushcricket tympana and adjacent septum may well serve the same purpose.

The authors admit that more work needs to be done to understand fully the complexity of the insect hearing organ, but they seem delighted with what they found:

This study has employed the opportunities for studying nonvertebrate hearing organs offered by OCT vibrometry. It revealed complexities in the micromechanics of the bushcricket CA that had not been found with previous methods. On the one hand, these findings bring new challenges in understanding insect hearing. On the other, they offer new views and suggest new solutions to known fundamental problems, including the delivery path of acoustic energy to the sensory tissue, the biophysics of auditory frequency selectivity, and the exact mechanisms that drive transduction.

These findings challenge Darwinism because species that are clearly unrelated by common ancestry employ common engineering principles. While the organs differ in size and construction, they are analogous in their physical operations: signal transduction, impedance matching, and frequency tuning. Even parts can be compared, like the vertebrate eardrum and the bushcricket tympanum, or the vertebrate hair cells and the insect sensory dendrites. Each implementation is ideally suited for the particular lifestyle of insects and vertebrates.

No Free Lunch

On ID the Future, Robert Marks and Eric Cassel (author of the new book Animal Algorithms) share a humorous story of trying to solve a Rubik’s cube blindfolded. By contrast, a teenager with eyes wide open and knowledge of the target configuration can solve the cube in seconds. Marks and Cassell discuss how the “no free lunch” theorems show that blind search will never solve complex problems like creating algorithms. An algorithm implies understanding a problem and designing a path to solve it. How much more knowledge and foresight does it take to design an entire system, a miniature acoustic organ that can receive, process, and transduce faint pressure waves into the sensation of sound?