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. 2021 Jun;529(8):1779-1786.
doi: 10.1002/cne.25056. Epub 2020 Oct 26.

Evolutionary and homeostatic changes in morphology of visual dendrites of Mauthner cells in Astyanax blind cavefish

Zainab Tanvir  1 , Daihana Rivera  1 , Kristen E Severi  1 , Gal Haspel  1 , Daphne Soares  1
Affiliations

Evolutionary and homeostatic changes in morphology of visual dendrites of Mauthner cells in Astyanax blind cavefish

Zainab Tanvir et al. J Comp Neurol. 2021 Jun.

Abstract

Mauthner cells are the largest neurons in the hindbrain of teleost fish and most amphibians. Each cell has two major dendrites thought to receive segregated streams of sensory input: the lateral dendrite receives mechanosensory input while the ventral dendrite receives visual input. These inputs, which mediate escape responses to sudden stimuli, may be modulated by the availability of sensory information to the animal. To understand the impact of the absence of visual information on the morphologies of Mauthner cells during developmental and evolutionary time scales, we examined the teleost Astyanax mexicanus. This species of tetra is found in two morphs: a seeing surface fish and a blind cavefish. We compared the structure of Mauthner cells in surface fish raised under daily light conditions, in surface fish raised in constant darkness, and in two independent lineages of cave populations. The length of ventral dendrites of Mauthner cells in dark-raised surface fish larvae were longer and more branched, while in both cave morphs the ventral dendrites were smaller or absent. The absence of visual input in surface fish with normal eye development leads to a homeostatic increase in dendrite size, whereas over evolution, the absence of light led to the loss of eyes and a reduction in dendrite size.

Keywords: adaptation; evolution; fish; homeostasis; neuron.

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Conflict of interest statement

Disclosure Statement

The authors have no conflicts of interest to declare.

Figures

Figure 1:
Figure 1:
Distribution and morphology of Astyanax mexicanus morphs used in this study. (a) Tinaja and Pachón morphs are geographically isolated in caves with these names in the Sierra del Abra region of Mexico (Tinaja: 22°04’34”N 98°58’40”W; Pachón: 22°36’25”N 99°02’55”W). Blue lines represent rivers in the area inhabited by the surface morph. Images from Google Earth. (b) Surface fish have pigmented eyes and skin, whereas Tinaja cavefish only have pigmented pupils and Pachón cavefish have no pigment on their skin or eyes. 7 dpf larvae. Common scale bar: a. 10 km b. 0.5 mm.
Figure 2:
Figure 2:
Neuronal morphology differs among Mauthner cells in surface fish raised in different light conditions, and in Tinaja and Pachón cavefish. Volume rendering of representative right Mauthner cells of (a) surface fish raised in 12L:12D conditions, note the ventral dendrite (VD) and two dendritic tips; (b) Mauthner cell of surface fish raised in 24D conditions, note four dendritic tips on the ventral dendrite. (c) Mauthner cell of Tinaja cavefish, note the ventral dendrite is smaller than those of surface fish. (d) Mauthner cell of Pachón cavefish, note the absence of ventral dendrite. VD: ventral dendrite, LD: lateral dendrite, So: soma, Ax: axon, arrowheads: dendritic tips. All neurons from 5 dpf larvae. Scale bar: 20 μm.
Figure 3:
Figure 3:
Mauthner cell ventral dendrites of surface fish increase in length and number of branches when raised in 24D conditions, while cavefish dendrites are smaller or absent. (a) Maximum dendritic length. (b) Number of dendritic tips. (c) Maximum dendritic diameter. (d) Length of primary branch. Three comparisons against the shared control surface (Sur.) 12L:12D are shown in Cumming estimation plots in which the raw data is plotted on the upper axes. On the lower axes, mean differences are plotted as bootstrap sampling distributions, each mean difference is depicted as a dot, and each 95% confidence interval is indicated by the ends of the vertical error bars. The numbers of neurons (animals) are Surface (Sur.) 12L:12D: n= 7 (5), Surface (Sur.) 24D: n= 6 (3), Tinaja: n= 8 (5), Pachón: n= 7 (4).
Figure 4:
Figure 4:
Mauthner cell morphology is variable among morphs and experimental conditions. (a1-a6) Surface 12L:12D (b1-b5) Surface 24D (c1-c7) Tinaja (d1-d6) Pachón. Scale bar: 20 μm.
Figure 5:
Figure 5:
Lateral dendrites are similar in length among all groups, but LD of surface fish larvae raised in 12L:12D are thinner than those of larvae raised in 24D and thicker than those of Pachón. (a) Maximum length of lateral dendrites. (b) Maximum diameter of lateral dendrites. Three comparisons against the shared control Surface (Sur.) 12L:12D are shown in Cumming estimation plots in which the raw data is plotted on the upper axes. On the lower axes, mean differences are plotted as bootstrap sampling distributions, each mean difference is depicted as a dot, and each 95% confidence interval is indicated by the ends of the vertical error bars. The numbers of neurons (animals) are Surface (Sur.) 12L:12D: n= 7 (5), Surface (Sur.) 24D: n= 4 (2), Tinaja: n= 6 (4), Pachón: n= 7 (4).
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