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.

Possible Molecular Mechanisms for Paramecium Learning

“…There are also different types of ciliates that exert phototactic behavior without the presence of stigma [43][44][45]. The mechanism of steering in ciliates is still unknown but it has been suggested that there are light sensing vesicles that form an independent miniature stigma with their associated cilia [40].…”

“…It is evident that eukaryotes have achieved the capability of phototaxis independently for at least eight times [40] and it is not difficult to achieve such a capability [40]. It has been suggested that chromalveolates (the eukaryotic supergroup that includes ciliates) were ancestrally photosynthesic and lost their red algal symbiont during their evolution [41].…”

“…It has been suggested that chromalveolates (the eukaryotic supergroup that includes ciliates) were ancestrally photosynthesic and lost their red algal symbiont during their evolution [41]. Many of the Alveolates (superphylum of the protozoan phylum Cilliophora) exert phototactic behavior and almost 5% of the species in this superphylum possess the stigma and they are mostly fresh water organisms [40] and even some have phototactic activity without any stigma [42]. In ciliates, phototactic behavior evolved independently from other chromalveolates [40].…”

Origin and early evolution of neural circuits for the control of ciliary locomotion

“…The best understood behaviour in protists is spiral vectorial phototaxis [33]. It can be found, among others, in the green alga Chlamydomonas [26], the excavate Euglena, the cryptophyte alga Cryptomonas [25], or in the ciliated spores of the chytrid fungi Allomyces [34].…”

“…Some animal larvae, such as sponges [36,37] and some cnidarians [38], perform phototaxis without a nervous system, while others, including some cnidarians [39] and many bilaterians [8,40], perform phototaxis with a nervous system. Phototaxis therefore provides a very useful paradigm to assess the benefits of nervous systems in a comparative framework, even if we are comparing independent evolutionary innovations [33].…”