Evolutionary convergence of a neural mechanism in the cavefish lateral line system
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Evaluation Summary:
This important and exciting paper demonstrates that the blind cavefish, known for its lack of eyes and increased number of lateral line hair cells, also exhibit physiological adaptations to increase lateral line sensitivity. The authors demonstrate that these adaptations have convergently evolved in multiple populations that have independently colonized cave environments. By leveraging the numerous strengths of the cavefish model, the authors are able to show precisely how neural circuits can be affected by adaptation to the environment.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1, Reviewer #2 and Reviewer #3 agreed to share their name with the authors.)
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Abstract
Animals can evolve dramatic sensory functions in response to environmental constraints, but little is known about the neural mechanisms underlying these changes. The Mexican tetra, Astyanax mexicanus , is a leading model to study genetic, behavioral, and physiological evolution by comparing eyed surface populations and blind cave populations. We compared neurophysiological responses of posterior lateral line afferent neurons and motor neurons across A. mexicanus populations to reveal how shifts in sensory function may shape behavioral diversity. These studies indicate differences in intrinsic afferent signaling and gain control across populations. Elevated endogenous afferent activity identified a lower response threshold in the lateral line of blind cavefish relative to surface fish leading to increased evoked potentials during hair cell deflection in cavefish. We next measured the effect of inhibitory corollary discharges from hindbrain efferent neurons onto afferents during locomotion. We discovered that three independently derived cavefish populations have evolved persistent afferent activity during locomotion, suggesting for the first time that partial loss of function in the efferent system can be an evolutionary mechanism for neural adaptation of a vertebrate sensory system.
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Author Response
Reviewer #1 (Public Review):
However, their rationale is weakened by the fact that the authors do not examine the number of mechanoreceptive hair cells (as a minimum) and their sensitivity to mechanical stimulation (ideally).
We have performed additional experiments to address these concerns. We found that hair cell quantities per neuromast are similar between surface and cavefish (Figure 1 F). We have also performed additional electrophysiological recordings to evaluate the mechanical sensitivity of the system. We also took the initiative to stimulate across several stimulus frequencies, which revealed that cavefish are more responsive at higher stimulus frequencies than surface fish (Figure 2 F).
I also did not quite like their use of "regression of the efferent system". In my opinion, this implies that the …
Author Response
Reviewer #1 (Public Review):
However, their rationale is weakened by the fact that the authors do not examine the number of mechanoreceptive hair cells (as a minimum) and their sensitivity to mechanical stimulation (ideally).
We have performed additional experiments to address these concerns. We found that hair cell quantities per neuromast are similar between surface and cavefish (Figure 1 F). We have also performed additional electrophysiological recordings to evaluate the mechanical sensitivity of the system. We also took the initiative to stimulate across several stimulus frequencies, which revealed that cavefish are more responsive at higher stimulus frequencies than surface fish (Figure 2 F).
I also did not quite like their use of "regression of the efferent system". In my opinion, this implies that the ancestral animals have a weak efferent system, which developed further in Astyanax (generally) and then regressed upon cave colonisation. I would have used another word that more precisely defines a weakening of activity.
We thank the reviewer for pointing this out and have replaced the term with the phrase “partial loss of function”.
I found it curious that the authors did not discuss the evident reduction of swim bout length in cavefish, compared to surface fish (F2Aii). Also, this difference seems not to correlate with motoneuron spike bout frequency. Perhaps the authors can add a sentence or two to discuss these issues, or simply explain to me if I got it wrong.
We thank the reviewer for bringing this to our attention. Exemplar traces (now Figure 3 Ai & Bi) were selected due to their similarity to each other in order to highlight the inhibition during swimming in surface fish and a loss of effect in cavefish. It was not meant to represent the population mean. The reviewer is correct, and we now report results from a new statistical analysis that confirms that cavefish do exhibit significantly shorter swim bout durations (264 ± 4 ms) compared to surface fish (357 ± 5ms).
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Evaluation Summary:
This important and exciting paper demonstrates that the blind cavefish, known for its lack of eyes and increased number of lateral line hair cells, also exhibit physiological adaptations to increase lateral line sensitivity. The authors demonstrate that these adaptations have convergently evolved in multiple populations that have independently colonized cave environments. By leveraging the numerous strengths of the cavefish model, the authors are able to show precisely how neural circuits can be affected by adaptation to the environment.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1, Reviewer #2 and Reviewer #3 agreed to share their name with the authors.)
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Reviewer #1 (Public Review):
The authors set out to investigate the possible adaptation of a sensory system to live in caves, where visual cues are strongly reduced or absent. In this case, although some light sensitivity may remain in blind populations of Astyanax, image-forming capabilities are entirely absent. Therefore, animals that need to determine their position relative to obstacles, find prey or escape from potential predators, may need to rely more heavily on mechanosensation. The question here is whether the lateral-line system has been modified to serve this need, and how so.
The major strength of the work is a clever choice of Astyanax populations, (three blind that independently colonised caves at different times) and one sighted (surface dwelling). The experiments are clean and sufficient to draw conclusions.
A weakness …
Reviewer #1 (Public Review):
The authors set out to investigate the possible adaptation of a sensory system to live in caves, where visual cues are strongly reduced or absent. In this case, although some light sensitivity may remain in blind populations of Astyanax, image-forming capabilities are entirely absent. Therefore, animals that need to determine their position relative to obstacles, find prey or escape from potential predators, may need to rely more heavily on mechanosensation. The question here is whether the lateral-line system has been modified to serve this need, and how so.
The major strength of the work is a clever choice of Astyanax populations, (three blind that independently colonised caves at different times) and one sighted (surface dwelling). The experiments are clean and sufficient to draw conclusions.
A weakness of the methods and results is that the authors choose to concentrate on the posterior lateral line upon the conclusion that because the number of neuromasts does not vary between cave and surface populations, any adaptation must occur elsewhere. However, their rationale is weakened by the fact that the authors do not examine the number of mechanoreceptive hair cells (as a minimum) and their sensitivity to mechanical stimulation (ideally). I also did not quite like their use of "regression of the efferent system". In my opinion, this implies that the ancestral animals have a weak efferent system, which developed further in Astyanax (generally) and then regressed upon cave colonisation. I would have used another word that more precisely defines a weakening of activity.
The results support the conclusions of the paper, but I am not entirely convinced by their assertion that "elevated afferent activity underlies the increased responsiveness of cavefish to flow stimuli". First, what do they mean by "responsiveness of cavefish to flow stimuli"? Is it reduced limen, elevated frequency of responses (across trials in individuals or and within a population)? Also, I am not familiar with the cave system. But is there any actual eater flow in caves? Perhaps the fish do not actually detect flow, but pressure distributions to enable the avoidance of obstacles.
I found it curious that the authors did not discuss the evident reduction of swim bout length in cavefish, compared to surface fish (F2Aii). Also, this difference seems not to correlate with motoneuron spike bout frequency. Perhaps the authors can add a sentence or two to discuss these issues, or simply explain to me if I got it wrong.
The work is very likely to have a significant impact in the field, and increase the overall interest in Astyanax as a valuable system for neurobiology and evolution.
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Reviewer #2 (Public Review):
Lunsford et al. reported a novel knowledge about the mechanism of sensitivity gaining in a sensory system, in which cavefish gained sensitivity likely due to attenuation of the afferent inhibition. This manuscript can potentially impact the neuroscience field by proposing a new mechanism for sensory gaining. This report also contains technical advancement in the cavefish system and excellent comparative data among surface and cave populations potentially impacting the evolutionary biology field.
The strength is that, by applying the fine neurophysiological technique, the authors first found that cavefish increased spontaneous activities in the afferent inputs from the mechanosensory lateral line to the brain. They also found that cavefish regress the inhibitory efferent signal from the brain to the …
Reviewer #2 (Public Review):
Lunsford et al. reported a novel knowledge about the mechanism of sensitivity gaining in a sensory system, in which cavefish gained sensitivity likely due to attenuation of the afferent inhibition. This manuscript can potentially impact the neuroscience field by proposing a new mechanism for sensory gaining. This report also contains technical advancement in the cavefish system and excellent comparative data among surface and cave populations potentially impacting the evolutionary biology field.
The strength is that, by applying the fine neurophysiological technique, the authors first found that cavefish increased spontaneous activities in the afferent inputs from the mechanosensory lateral line to the brain. They also found that cavefish regress the inhibitory efferent signal from the brain to the mechanosensory lateral line, in which the efferent inhibits the afferent signal. This inhibition is typical in the fish system to mask the lateral line/flow sensing information during the tail-beating. Cavefish seemed to reduce the efferent signal; then the authors argue that cavefish gained the lateral line sensitivity more.
The weakness is that the authors did not show the relationship between sensitivity and spontaneous activities in the afferents. The signal/noise ratio (S/N ratio) is important where the animal can be aware of the actual signals from the environment out of the noisy self-generating spontaneous signals (but c.f. stochastic resonance). As far as I read, this study misses the comparison between the signal and the spontaneous spikes, or any other alternatives that support their conclusion: cavefish gained higher sensitivity.
If the authors address this point, I believe this study has a strong scientific impact on neurophysiology and evolutionary biology to show how animals evolved higher sensing ability. -
Reviewer #3 (Public Review):
Lunsford et al. investigated the neurophysiological activity of posterior lateral line afferent neurons between surface and cave populations of the Mexican tetra A. mexicanus. Cave populations of A. mexicanus show heightened lateral line sensitivity, which has been attributed in part to the increased number of neuromasts in the anterior lateral line. The authors of this study exploit a key developmental difference in larval cavefish: the density of posterior lateral line neuromasts is not significantly different between cave and surface populations. Using this key observation, the authors demonstrate several key findings: First, Pachon cavefish neuromast afferents exhibit significantly higher spontaneous activity. Second that Pachon cavefish do not decrease afferent activity during bouts of fictive swimming, …
Reviewer #3 (Public Review):
Lunsford et al. investigated the neurophysiological activity of posterior lateral line afferent neurons between surface and cave populations of the Mexican tetra A. mexicanus. Cave populations of A. mexicanus show heightened lateral line sensitivity, which has been attributed in part to the increased number of neuromasts in the anterior lateral line. The authors of this study exploit a key developmental difference in larval cavefish: the density of posterior lateral line neuromasts is not significantly different between cave and surface populations. Using this key observation, the authors demonstrate several key findings: First, Pachon cavefish neuromast afferents exhibit significantly higher spontaneous activity. Second that Pachon cavefish do not decrease afferent activity during bouts of fictive swimming, as do surface and other 'sighted' fish like zebrafish. This is presumably due to the absence of a corollary discharge signal produced by motor activity: the authors demonstrate this is the case by ablating efferent neurons in the hindbrain of both cave and surface fish, showing that surface fish afferents no longer decrease their firing rate during swimming, whereas cavefish are unaffected by the ablation. Finally, leveraging a key strength of the cavefish model, the authors examine three populations that have independently colonized caves from surface populations, demonstrating that the same general effect as found in Pachon cavefish, with interesting variation in the Molino cave.
This is an exciting and important paper to those seeking to understand the evolution of sensory systems and their adaptation to different environments. The paper is exceptionally well written, with clear and beautiful figures. It applies widely used neurophysiological techniques in zebrafish to an increasingly important evolutionary model A. mexicanus. By exploiting key developmental and population-level differences, the authors demonstrate plausibly adaptive differences in neural circuits, not just those due to external morphology. These findings motivate a series of exciting hypotheses for future studies, including hypotheses about sensory function in other lineages of troglodytic fish.
Overall, the studies described in this manuscript are simple and elegant, however require familiarity with the neural circuitry of the lateral line to understand the experiments. This could be improved in the introductory materials and potentially through an explanation of the terms labeled in figure 3Ci and 3Cii. Second, while a major finding of the paper, little attention is paid to potential mechanisms to explain the increased spontaneous activity of neuromasts in multiple populations of cavefish. While it is clear that both CD inactivity and increased spontaneous activity will lead to increased lateral line sensitivity, some assessment of the relative importance of these two phenomena would be useful. Given that ablated surface fish survive according to the methods, it seems that experimenters have larval fish lacking CD, but with lower spontaneous afferent activity. Some comparison of spontaneous swimming activity between these manipulated groups could have provided some additional insight. These concerns are relatively minor to an otherwise excellent and exciting paper.
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