Blind cavefish: social butterfly or awkward turtle?

By Nour Bundogji (Pitzer College), Niti Nagar (Claremont McKenna College), and Sachin Shah (Claremont McKenna College) [Edited by Lars Schmitz, as part of BIOL 167 “Sensory Evolution”, an upper division class at the W.M. Keck Science Department. Written for educational purposes only].

Would you have ever guessed that the evolution of sensory systems may dictate your social behaviors? Well, this certainly seems to be the case for cavefish, Astyanax mexicanus. Many studies have shown that fish are quite social creatures. In fact, Anna Greenwood, a scientist in the Human Biology Division at Fred Hutchinson Cancer Research Center said, “the motivation to be social is common among fish and humans, where some of the same brain regions and neurological chemicals that control human social behavior are probably involved in fish social behavior.” The two types of social behaviors that A. mexicanus exhibit are schooling and shoaling. As part 1 of an amazing twin paper in Current Biology, Kowalko and colleagues (2013) distinguished between these two behaviors by defining schooling as the tendency of fish to synchronize their behavior and swim together, while shoaling is the tendency of fish to group with other fish of the same species.  Both these social behaviors provide a number of advantages such as deterring attacks from predators and foraging for food.

Figure 1. Beautiful Mexican blind cavefish. [By H. Zell (Own work) [GFDL (http://www.gnu.org/copyleft/fdl.html) or CC-BY-SA-3.0 (http://creativecommons.org/licenses/by-sa/3.0)], via Wikimedia Commons]

Figure 1. Beautiful Mexican blind cavefish. [By H. Zell (Own work) [GFDL (http://www.gnu.org/copyleft/fdl.html) or CC-BY-SA-3.0 (http://creativecommons.org/licenses/by-sa/3.0)%5D, via Wikimedia Commons]

In this study, several populations of A. mexicanus (Figure 1) were used to investigate the mechanism responsible for loss of schooling and shoaling behaviors: the sighted surface dwelling and three independently evolved blind cave-dwelling fish (Tinaja, Pachon, and Molino populations).

So, what exactly are the reasons behind the absence of schooling and shoaling behavior in cavefish? Kowalko and colleagues proposed four hypotheses behind this loss. For example, it may be due to the absence of large predators in caves, which minimizes the need for fish to travel close together in schools. In addition, food is fairly scarce in many caves, which may make these behaviors unfavorable. This loss could otherwise be due to the fact that cavefish have lateral line systems that are different from their surface dwelling counterparts. Lastly, the disappearance of this behavior may be due to genetic components that are independent of vision loss.

Kowalko and her fellow researchers first investigated the differences in schooling and shoaling behaviors in the two types of A. mexicanus. They measured schooling by recording the tendency of fish to follow a model school of plastic fish (Figure 2).  The surface fish followed the model school and the three independently evolved cavefish did not display any schooling behaviors.

Figure 2. Kowalko et al. designed this apparatus shown above to measure schooling behavior [from Kowalko et al., 2013]

Figure 2. Kowalko et al. designed this apparatus shown above to measure schooling behavior [from Kowalko et al., 2013]

Tests for shoaling were integrated in the tests for schooling where the researchers measured the average distance to the nearest fish. They found that surface fish swam closer together than any other cavefish population (Figure 3).

Figure 3. Shoaling was measured by quantifying the average nearest neighbor distance and average inter-individual distance. Results show surface swam closer together than any other cavefish. Thus, cavefish have lost the tendency to school or shoal. [from Kowalko et al., 2013]

Figure 3. Shoaling was measured by quantifying the average nearest neighbor distance and average inter-individual distance. Results show surface swam closer together than any other cavefish. Thus, cavefish have lost the tendency to school or shoal. [from Kowalko et al., 2013]

Surface fish show aggregating behavior even when they are raised in isolation, so there must be some kind of genetic determination of this behavior. When looking at the genetics of schooling behavior, the Kowalko team crossed surface fish with Tinaja cavefish to determine whether this trait was dominant or recessive. The F1 generation of fish portrayed that schooling is a dominant behavior. However, the F2 generation revealed fish with schooling and non-schooling behaviors indicating social behavior has a polygenic basis.

Cavefish have larger number and size of cranial neuromasts in comparison to surface fish (Yoshizawa et al., 2014). Kowalko and his fellow researchers used a similar reasoning to test their lateral line hypothesis by comparing the number of neuromasts to the proportion of time spent schooling and shoaling for both surface and cavefish. However, they failed to find a relationship between the two, concluding that cave environments do not have an effect on the evolutionary loss of these behaviors.

So, what is responsible for the loss of schooling and shoaling? To determine this, they tested whether loss of schooling would be seen in cavefish that lost visual function during development. Removing one lens from surface fish larvae produced a significant effect on shoaling behavior such that fish swam farther away from one another. When surface fish had both lenses removed, they schooled significantly less from those with one lens removed. Thus, it was concluded that vision is essential for schooling and shoaling behaviors (Figure 4).

Figure 4. Variation of lenses in surface fish (C-E) compared to cavefish (F). Lens removal resulted in less social behavior (G,H). [from Kowalko et al., 2013]

Figure 4. Variation of lenses in surface fish (C-E) compared to cavefish (F). Lens removal resulted in less social behavior (G,H). [from Kowalko et al., 2013]

To further investigate this finding, these researchers looked at visual function, defined as the ability to sense light. This was compared between the F1 generation, cavefish, and surface fish. The surface fish and the F1hybrids spent most of their time in the dark (avoiding the light), indicating their ability to detect light. On the other hand, the cavefish did not indicate a preference for the light or dark environment, indicating their inability to detect light. Many non-schooling fish have little visual function, as they display no light preference. However, some light detecting fish do not show schooling behavior, suggesting that there may be a visually independent component to schooling and shoaling.

Overall, vision seems to be the determining factor responsible for these behaviors in fish. This indicated that the evolution of sensory systems can contribute to the complexity of social behaviors in vertebrates. In this study, it was further suggested that two eyes are responsible for following the haphazard movement of fish, which is important for maintaining normal schooling and shoaling behaviors.

Although the researchers were effective in showing the importance of vision-dependent mechanisms in social behavior, there were some minor shortcomings to their investigation, leaving room for future studies. Previous work has shown that experimentally blinded surface fish exhibit schooling behaviors, which contradicts results found in this study (Partridge and Pitcher, 1980). This discrepancy suggests that further studies investigating visual-independent factors should be conducted to confirm either finding. For example, this study did not account for discrepancies in habitats or other selective mechanisms, such as the presence of predators or the scarcity of food. Furthermore, only Tinaja cavefish were tested when examining the effect of the lateral line system. It was also found last year that benthic sticklebacks (another really important species for understanding evolution; see Greenwood et al. 2013 — part 2 of the twin paper!) displayed differences in social behavior dependent on the evolution of the lateral line system, which wasn’t the case for A. mexicanus. Thus, it would be advantageous to conduct the same lateral line system test for more cavefish populations and other species.

References

Greenwood, A. K., Wark, A. R., Yoshida, K., Peichel C. L. 2013. Genetic and neural modularity underlie the evolution of schooling behavior in Threespine Sticklebacks. Current Biology 23: 1884-1888. (DOI: 10.1016/j.cub.2013.07.058)

Kowalko, J.E., Rohner, N., Rompani, S. B., Peterson, B. K., Linden, T. A., Yoshizawa, M., Kay, E. H., Weber, J., Hoekstra, H. E., Jeffery, W. R., Borowsky, R., T., Clifford J. 2013. Loss of schooling behavior in cavefish through sight-dependent and sight-independent mechanisms. Current Biology 23, 1874-1883. (DOI: 10.1016/j.cub.2013.07.056).

Partridge, B. L., Pitcher, T. J. 1980. The sensory basis of fish schools: roles of lateral line and vision. Journal of Comparative Physiology 135, 315-325. (DOI: 10.1007/BF00657647).

Yoshizawa, M., Jeffery, W. R., van Netten, S. M., McHenry, M. J. 2004. The sensitivity of lateral line receptors and their role in the behavior of Mexican blind cavefish (Astyanax mexicanus). Journal of Experimental Biology 217: 886. (DOI: 10.1242/​jeb.094599).

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