Let your neurons relax, the predators are gone!

Predators eat prey. Prey, over time, evolve features to evade predators. But what happens when predators go away?

This paper by Fullard and colleagues is almost a perfect storm of topics that I’ve talked about several times before on this blog. We got crickets (previous appearances here, here, and here), we got bats (previous appearances here and here), we got reverse evolution (discussed here).

Teleogryllus oceanicus is found on landmasses across the Pacific Ocean, ranging from mainland Australia to remote islands. The distances between populations are so large that you would expect these populations to be slowly separating by genetic drift alone. Using highly variable regions of DNA, Fullard and colleagues showed that there were genetic differences in the crickets based on the geographic distance between them. The most distinct populations were from the Australia city of Darwin, and Moorea in French Polynesia. While a few people might know Darwin is located in Australia’s top end, I expect very few could pinpoint Moorea on a map, so I’ve done it for you. Moorea’s the one on the right.


Not only is it a bit tricky for humans to locate, being far in the middle of the Pacific Ocean, bats haven’t located it either. There are no bats living on Moorea, in contrast to the Australia mainland, which boasts a rich assemblage of the flying mammals. Bats are cricket predators, So this creates an interesting situation where there are expected to be clear differences in selection pressure on the crickets. Many aspects of crickets’ sensory systems, particularly hearing, seem to be specifically tuned to detecting and avoiding bats. Several big auditory neurons respond strongly to the ultrasound that bats make when echolocating, and crickets will fly away from ultrasound pulses (negative phonotaxis).

One critical neuron that crickets use, in some contexts, as a bat detector: ascending neuron 2 (mentioned before here; red in the picture). Ascending neuron 2 (AN2) isn’t the only auditory interneuron that can respond to high frequency bat sounds that bats make when echolocating, however. Another neuron is omega neuron 1 (ON1), which responds both to high frequency, bat-like sounds, but it also critical to the processing of low-frequency, cricket like sounds (green in the picture).

Thus, the prediction from evolutionary theory is that in a situation with no bats, you would expect there to be reduced selection pressure to maintain the neurons’ sensitivity to high-frequency, bat-like sounds. The decrease in selection pressure should be stronger for AN2 than ON1, because AN2 seems to be more strongly dedicated to a single task than ON1.

There are many different parameters of a neuron’s response to a stimulus, but the authors present for sensitivity: What is the lowest level of sound needed to get the neuron to fire? The Moorea population’s threshold for AN2 is significantly higher across the board, whereas the sensitivity for ON1 is not significantly different at almost every frequency. There is a significant difference at one frequency, 15 kHz, but this seems to be a chance finding due to the large number of comparisons being made.

This difference is also reflected in the behaviour. There was no significant difference between the populations in turning towards a cricket-like low-frequency sound, but there is a significant difference in populations when turning away from bat-like high-frequency sound.

What this paper doesn’t have is a good description of the suspected history of cricket colonization or bat colonization across the range. This is probably because it is unknown, but it would be interesting to have some idea of how long the crickets in French Polynesia may have been in a bat-free environment.

A great follow-up study would be to look at what level this evolutionary change has occurred at. There are many ways that an interneuron could lose sensitivity to a stimulus. The ear could change; the sensory neurons in the ear could change; the connections of the sensory neurons to the interneurons; the physiology of the interneuron could change... and so on.

Full disclosure: One of the authors here was my boss about a decade ago. I wish he’d been working on this project then!

Reference

Fullard, J., Hofstede, H., Ratcliffe, J., Pollack, G., Brigidi, G., Tinghitella, R., & Zuk, M. (2009). Release from bats: genetic distance and sensoribehavioural regression in the Pacific field cricket, Teleogryllus oceanicus Naturwissenschaften DOI: 10.1007/s00114-009-0610-1

Neuron picture from Scholarpedia.