Our evolutionary model can be tested both morphologically and molecularly. It predicts that despite their different, segregated functions, the distinct cell types making up the multicellular metazoan phototaxis system should show morphological resemblances and vestiges reflecting their common evolutionary ancestry. We can envisage that in some cases, the functionally segregated sister cell types should show residual functions (which they had otherwise lost), reflecting the ancient multicellular state. A literature survey reveals that such cell types indeed exist in the eyespots of invertebrate larvae and adults, both in the form of PRCs retaining some shading pigment and SPCs retaining small sensory organelles.
In several species of the polychaete Saccocirrus
, the SPC exhibits an apical extension with some rhabdom-like microvilli and vestigial cilia (a
; Eakin et al. 1977
; Purschke 1992
; Purschke et al. 2006
). In these species, both SPC and PRC are part of the epidermal layer and the eye cup opens to the exterior. Both cells form axon-like processes that are closely aligned and enter the neuropil of the brain. A similar observation has been made regarding the adult eyes of the annelid S. armiger
, which possess an SPC with a dense array of microvilli presumed to be sensory (Wilkens & Purschke in press
). Adding to this, the SPC of the larval eye in Platynereis
and in the sedentary Cirratulidae, as well as of the bicellular ocelli of Saccocirrus
, send out sensory axons at later developmental stages (G. Purschke, H. Hausen & D. Arendt 2009, unpublished data), corroborating the (hidden) sensory nature of these cells.
Figure 4. (a) Two-celled eye of Saccocirrus papillocercus after transmission electron microscopy observations. PRC and SPC are embedded in the layer of epidermal cells (EPCs); both cells with microvilli (mv) in rhabdomeric arrangement, vestigial cilia (arrowheads) (more ...)
It is well established that PRCs show characteristics of SPCs to various extents. For example, pigment vesicles have been found in cephalopod (Yamamoto et al. 1965
; Budelmann et al. 1997
) and gastropod eyes (Blumer 1999
; Zhukov et al. 2006
) and appear to be a common feature of annelids with multicellular adult eyes, as observed in the Platynereis
adult eye PRCs (Rhode 1992
); at least in Phyllodocida and Eunicida, this very likely belongs to the ground pattern of eyes, and in these taxa, the absence of pigment vesicles may be interpreted as a secondary character state (Suschenko & Purschke 2009
). In line with a general affinity of PRC and SPC, the retina of the Patella
eye is exclusively composed of pigmented PRCs (b
Finally, the more or less reduced accessory cilium that is usually present in annelid rhabdomeric PRCs of adult eyes (see, for example, Purschke 2005
) can be interpreted as the remnants of a former locomotor function. Unfortunately, up to now, nothing is known about the function of any of these accessory cilia.
Corroborating the affinity of PRCs and SPCs, we have determined the molecular fingerprint of cell types making up the larval and adult eyes of Platynereis
(Guy et al. submitted
) and found that the rhabdomeric PRC and the SPC of the larval eyes are more closely related to each other than they are to their functional counterparts in the adult eye or to any other cell of the developing larval episphere. Both cell types specifically express the combination of the transcription factors pax6, lhx2, sim
, as their regulatory signature, and the acetylcholine receptor AChR7/8, which confer a unique molecular fingerprint to these cells (Arendt 2008
). None of these genes is expressed in the PRCs or SPCs of the adult eyes. The latter, in turn, express the transcription factors six1/2, eyes absent, dachshund
, plus the sepiapterin synthase A
, a key enzyme in the synthesis of the shading pigment. Again, none of these genes is active in the larval eyes. These data suggest that the PRCs and SPCs of the larval eyes and those of the adult eyes have evolved by cell-type functional segregation in two independent evolutionary events.