Cytological Basis of Photoresponsive Behavior in a Sponge Larva

Abstract

Ontogenetic changes in the photoresponse of larvae from the demosponge Reneira sp. were studied by analyzing the swimming paths of individual larvae exposed to diffuse white light. Larvae swam upward upon release from the adult, but were negatively phototactic until at least 12 hours after release. The larval photoreceptors are presumed to be a posterior ring of columnar monociliated epithelial cells that possess 120-microm-long cilia and pigment-filled protrusions. A sudden increase in light intensity caused these cilia to become rigidly straight. If the light intensity remained high, the cilia gradually bent over the pigmented vesicles in the adjacent cytoplasm, and thus covered one entire pole of the larva. The response was reversed upon a sudden decrease in light intensity. The ciliated cells were sensitive to changes in light intensity in larvae of all ages. This response is similar to the shadow response in tunicate larvae or the shading of the photoreceptor in Euglena and is postulated to allow the larvae to steer away from brighter light to darker areas, such as under coral rubble-the preferred site of the adult sponge on the reef flat. In the absence of a coordinating system in cellular sponges, the spatial organization and autonomous behavior of the pigmented posterior cells control the rapid responses to light shown by these larvae.

The ‘division of labour’ model of eye evolution

“…Note the absence of microvilli. After Leys & Degnan (2001) and Maldonado et al (2003). (b) Rhabdomeric PRC in the planula larva of the cubozoan cnidarian Tripedalia; rhabdomeric microvilli (mv) shaded from various directions (Nordstrom et al 2003).…”

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

“…An analogous spiral swimming phototactic strategy is found in the multicellular green alga Volvox [35], and also in the ciliated larvae of animals including sponges [36,37], cnidarians [38,39], annelids [8] and molluscs [40]. 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].…”

“…Such a transformation probably also happened in the case of photoreceptors, which started as cell-autonomous sensory-motor units [36,38,44] and evolved into sensorymotor neurons regulating ciliary bands (figure 2b). We argued recently that the sensory-motor phototactic eyes, directly synapsing on ciliated cells in the larvae of the annelid Platynereis represent such an ancestral stage in eye circuit evolution [8].…”

“…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]. An analogous spiral swimming phototactic strategy is found in the multicellular green alga Volvox [35], and also in the ciliated larvae of animals including sponges [36,37], cnidarians [38,39], annelids [8] and molluscs [40]. 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.…”

“…Sensory cells evolved in the first metazoans before the origin of bona fide neurons [36,37,41]. Sponge larvae have flask-shaped sensory cells (additional to their photoreceptors), embedded in an epithelial layer of polarized, ciliated cells [36].…”