Visual opsin expression and morphological characterization of retinal photoreceptors in the pouched lamprey (Geotria australis, Gray)

Abstract

Lampreys are extant members of the agnathan (jawless) vertebrates that diverged ~500 million years ago, during a critical stage of vertebrate evolution when image‐forming eyes first emerged. Among lamprey species assessed thus far, the retina of the southern hemisphere pouched lamprey, Geotria australis, is unique, in that it possesses morphologically distinct photoreceptors and expresses five visual photopigments. This study focused on determining the number of different photoreceptors present in the retina of G. australis and whether each cell type expresses a single opsin class. Five photoreceptor subtypes were identified based on ultrastructure and differential expression of one of each of the five different visual opsin classes (lws, sws1, sws2, rh1, and rh2) known to be expressed in the retina. This suggests, therefore, that the retina of G. australis possesses five spectrally and morphologically distinct photoreceptors, with the potential for complex color vision. Each photoreceptor subtype was shown to have a specific spatial distribution in the retina, which is potentially associated with changes in spectral radiance across different lines of sight. These results suggest that there have been strong selection pressures for G. australis to maintain broad spectral sensitivity for the brightly lit surface waters that this species inhabits during its marine phase. These findings provide important insights into the functional anatomy of the early vertebrate retina and the selection pressures that may have led to the evolution of complex color vision.

The Functional Anatomy of the Cornea and Anterior Chamber in Lampreys: Insights From the Pouched Lamprey, Geotria australis (Geotriidae, Agnatha)

“…The image-forming eyes of G. australis have been found to be the most specialised of all lampreys examined, at least with respect to photoreception. In contrast to the northern hemisphere (holarctic) lampreys and members of the only other southern hemisphere family of lampreys (Mordaciidae), the pouched lamprey possesses five types of photoreceptors (based on both morphology, spectral sensitivity and visual opsin expression, Collin et al, 2003a , b ; Warrington et al, 2020 ), providing the potential for pentachromatic vision under some light conditions throughout its protracted life cycle. The eyes of members of the holarctic Petromyzontidae possess two photoreceptor types (a cone-like and a rod-like, Holmberg et al, 1977 ; Ishikawa et al, 1987 ), while the Mordaciidae possess only a single type of rod-like photoreceptor ( Collin and Potter, 2000 ).…”

Vision and retina evolution: How to develop a retina

“…Lampreys ( Fig. 3 ) express up to five different sensory cells ( Collin et al, 2009 , Warrington et al, 2021 ) with morphology resembling that of jawed vertebrates ( Lamb, 2013 , Lamb et al, 2007 ). One sensory cell type expresses rhodopsin and shows rod-like transduction ( Lamb, 2013 ) yet also shows cone-like light saturation dynamics ( Fain, 2019 , Morshedian and Fain, 2017 ).…”

Interphotoreceptor coupling: an evolutionary perspective

“…Clearly, mixing the signals generated by cones of different spectral type via gap junctions prior to the decoding step should be detrimental to colour discrimination [57,58] and, therefore, disfavoured in evolution. This constraint is likely to have been already present in our last common ancestor with lampreys, since some species of this agnatan (jawless vertebrate) possess the substrate for sophisticated colour discrimination [133]. An animal in which much effort has been dedicated to examine whether cone-cone coupling adheres to this expectation is the turtle.…”