By Jessica Valenzuela (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].
As humans, we oftentimes think of vision as the primary sense, since it is what we rely on most heavily to provide us with information about our environment. But what happens when an animal is blind? What sense takes over, if any? In the case of the Astyanax mexicanus, or the Mexican tetra, it is believed that their chemosensory abilities, particularly olfaction, have become specialized to compensate for the loss of eyes.
Surprisingly, not all Astyanax mexicanus are completely eyeless. Members of this species are found in two morphs: surface dwelling, with eyes and pigmentation, or cave dwelling, without eyes or pigmentation (Romero, 1984). In this case, the cave morph fish display true troglomorphy, a drastic change in their traits that allows for permanent life in subterranean environments, whereas the surface morph show no change, since they live aboveground and only spend a short amount of time in subterranean habitats (Soares and Niemiller, 2013). Interestingly enough, when the two morphs breed, they produce viable hybrid offspring that range in their degree of troglomorphy – best determined by the size of eyes – with some having pigmentation and no eyes, eyes and no pigmentation, or a wide range of pigmentation and eye size (Bibliowicz et al., 2013).It was this unique population of Mexican tetra, illustrated in Figure 1, that made the 2013 experiment conducted by Bibliowicz et al. possible. In this study, the chemosensory abilities of a population of Mexican tetra from the Rio Subterráneo cave in Mexico were tested to determine whether or not the olfactory system underwent adaptive changes to allow the cave-dwelling morph to forage in the absence of light (Bibliowicz et al., 2013). Previous studies maintain that the cave morph fish possesses a higher number of superficial neuromasts and taste buds, indicating a modification of other sensory systems in the cave-dwelling Mexican tetra, namely, the lateral line and taste buds (Franz-Odendaal and Hall, 2006).
Unlike these studies, Bibliowicz et al. did not study the lateral line or taste buds but conducted a pioneer experiment that focused on the olfactory aspect of chemosensation. The team minimized the disturbance to the fish by conducting the experiment in the fish’s natural habitat rather than a lab and using a night vision camera in place of lights. The olfactory stimulus was then introduced by dripping granular food solvent into one corner of the pool where the fish were placed (Figure 2). Water was dripped in the other corner of the pool to account for any attraction the fish may have had to the vibrations in the water caused by the drip of liquid. Olfactory effectiveness for each morph was measured by comparing the time each fish spent near the food extract and determining the morph of each individual based on the video and their traits. It was found that the cave-like fish spent the most time near the extract while the surface-like fish did not even approach the area with the extract. This is a surprisingly drastic result, showing a clear correlation between the lack of eyes and the improved olfaction necessary to detect the food source (Bibliowicz et al. 2013).But what about the olfactory system changed in these eyeless Mexican tetras? The team that collaborated on the experiment measured the naris, or nostril (pl. ‘nares’), size of the fish relative to body length and found that those attracted to the food extract had small or no eyes and relatively large nares (Bibliowicz et al. 2013). This tells us that there is a correlation between eye loss and olfactory specialization and that naris size could play an important role in the enhancement of olfaction in cavefish. From an evolutionary standpoint, an improved olfactory system is the Mexican tetra’s form of compensation for the degradation or loss of vision. Particularly in the perpetually dark environment of caves, the early cave-dwelling ancestors would have no use for their eyes and have an increasing dependence on chemosensation for foraging and communication.
The ability of the Mexican tetra to express the entire range of its phenotypes, from the surface-dwelling morph to the various hybrids to the cave-dwelling morph, also makes it important for evolutionary studies. This unique morphological range makes it an ideal model organism for predicting the sensory adaptations and evolution of other cave-dwelling organisms. The spectrum of phenotypes seen in an extant population this one species is a sort of “evolution in action,” since the subtle changes in traits between the phenotypes would normally only occur through evolution over long periods of time in other species. In other words, it is an easily observable species for the evolution of sensory systems in response to the drastic change in environment between the surface and the cave. Amazingly enough, these observations can then be applied to other cave-dwelling organisms to make predictions, not only about their evolution and sensory adaptations, but also about what traits their ancestors may have expressed.
Although these findings are a step in the right direction in advancing our understanding of sensory system trade-offs in organisms, more research is needed to fully understand the modality of olfactory adaptation. A study should be conducted exploring the function of the naris in regards to olfaction and how size may influence olfactory sensitivity. Naris size has been shown in this study to play some role in the specialized olfaction; however, beyond that not much is known about the nares’ function in relation to olfaction. Additionally, the intermediate hybrid individuals should be studied more closely to obtain an understanding of the process of adaptation. With such a unique, extant population capable of expressing the entire spectrum of phenotypes, researchers could take the opportunity to use Mexican tetras as a model organism for understanding sensory trade-off and evolution in other cave dwelling organisms.
Bibliowicz, J., Alié, A., Espinasa, L., Yoshizawa, M., Blin, M., Hinaux, H., Legendre, L., Père, S., Rétaux, S. 2013 Differences in chemosensory response between eyed and eyeless Astyanax mexicanus of the Rio Subterráneo cave. EvoDevo 4:25 (DOI 10.1186/2041-9139-4-25)
Franz-Odendaal, T. A. and Hall, B. K. 2006 Modularity and sense organs in the blind cavefish, Astyanax mexicanus. Evolution & Development 8:94–100 (DOI 10.1111/j.1525-142X.2006.05078.x)
Hara, T. J. 1994. Olfaction and gustation in fish: an overview. Acta Physiol Scand 152, 207-217. ISSN 0001-6772. Canada Department of Fisheries and Oceans, Freshwater Institute, Canada
Romero, A. 1984. Behavior in an ‘intermediate’ population of the subterranean-dwelling characid Astyanax fasciatus. Environmental Biology of Fishes 80, 203-207.
Soares, D. and Niemiller, M. 2013 Sensory Adaptations of Fishes to Subterranean Environments. BioScience 63, 274-283. (DOI 10.1525/bio.2013.63.4.7)