Evolution of phototaxis

Abstract

Phototaxis in the broadest sense means positive or negative displacement along a light gradient or vector. Prokaryotes most often use a biased random walk strategy, employing type I sensory rhodopsin photoreceptors and two-component signalling to regulate flagellar reversal. This strategy only allows phototaxis along steep light gradients, as found in microbial mats or sediments. Some filamentous cyanobacteria evolved the ability to steer towards a light vector. Even these cyanobacteria, however, can only navigate in two dimensions, gliding on a surface. In contrast, eukaryotes evolved the capacity to follow a light vector in three dimensions in open water. This strategy requires a polarized organism with a stable form, helical swimming with cilia and a shading or focusing body adjacent to a light sensor to allow for discrimination of light direction. Such arrangement and the ability of three-dimensional phototactic navigation evolved at least eight times independently in eukaryotes. The origin of three-dimensional phototaxis often followed a transition from a benthic to a pelagic lifestyle and the acquisition of chloroplasts either via primary or secondary endosymbiosis. Based on our understanding of the mechanism of phototaxis in single-celled eukaryotes and animal larvae, it is possible to define a series of elementary evolutionary steps, each of potential selective advantage, which can lead to pelagic phototactic navigation. We can conclude that it is relatively easy to evolve phototaxis once cell polarity, ciliary swimming and a stable cell shape are present.

Figure 1.

The distribution of three-dimensional phototaxis in the tree of eukaryotes. Red arrows indicate the likely point of origin of phototaxis in a given group. Question marks indicate uncertainties regarding independent or common origin.

Figure 2.

The diversity of phototactic eukaryotes (a) a green alga (scale bar, 2 µm), (b) a heterokont zoospore, (c) a cryptomonad alga, (d) a dinoflagellate (scale bar, 10 µm), (e) Euglena (scale bar, 5 µm), (f) a chytrid zoospore (scale bar, 2 µm), (g) a sponge larva (scale bar, 100 µm), (h) a cnidarian larva (scale bar, 50 µm) and (i) a polychaete larva (scale bar, 50 µm).