Morphology and spectral absorption characteristics of retinal photoreceptors in the southern hemisphere lamprey (Geotria australis)

Abstract

The morphology and spectral absorption characteristics of the retinal photoreceptors in the southern hemisphere lamprey Geotria australis (Agnatha) were studied using light and electron microscopy and microspectrophotometry. The retinae of both downstream and upstream migrants of Geotria contained two types of cone photoreceptor and one type of rod photoreceptor. Visual pigments contained in the outer segments of these three photoreceptor types had absorbance spectra typical of porphyropsins and with wavelengths of maximum absorbance (downstream/upstream) at 610/616 nm (long-wavelength-sensitive cone, LWS), 515/515 nm (medium-wavelength-sensitive cone, MWS), and 506/500 nm (medium-wavelength-sensitive rod). A "yellow" photostable pigment was present in the myoid region of all three types of photoreceptor in the downstream migrant. The same short-wavelength-absorbing pigment, which prevents photostimulation of the beta band of the visual pigment in the outer segment, was present in the rods and LWS cones of the upstream migrant, but was replaced by a large transparent ellipsosome in the MWS cones. Using microspectrophotometric and anatomical data, the quantal spectral sensitivity of each photoreceptor type was calculated. Our results provide the first evidence of a jawless vertebrate, represented today solely by the lampreys and hagfishes, with two morphologically and physiologically distinct types of cone photoreceptors, in addition to a rod-like photoreceptor containing a colored filter (a cone-like characteristic). In contrast, all other lampreys studied thus far have either (1) one type of cone and one type of rod, or (2) a single type of rod-like photoreceptor. The evolution or retention of a second type of cone in adult Geotria is presumably an adaptation to life in the brightly lit surface waters of the Southern Ocean, where this species lives during the marine phase of its life cycle. The functional significance of the unique visual system of Geotria is discussed in relation to its life cycle and the potential for color vision.

Vision in the southern hemisphere lampreyMordacia mordax: Spatial distribution, spectral absorption characteristics, and optical sensitivity of a single class of retinal photoreceptor

“…Given the other retinal adaptations for increasing photon capture in M. mordax, another possible function for the large ellipsosome is to focus light onto the visual pigment within the outer segment. This would parallel the role played by (Holmberg & Öhman, 1976;Dickson & Graves, 1982, Petromyzontidae, A), the southern hemisphere lamprey Geotria australis , 2003a and Mordacia mordax (this study, Mordaciidae, C). The nomenclature for the five cone-like receptors (C1-C5) in G. australis follows that of Collin and Trezise (2004).…”

“…However, given that the true rod visual pigment (the opsin gene Rh1) has not been found in either of the two other families of lampreys (Petromyzontidae and Geotriidae) and that full scotopic (dim light, rod-based) vision is most likely only to have evolved after the separation of the jawed (gnathostomatous) vertebrates (Collin et al, 2003b;Collin & Trezise, 2004), the identity of the receptor type in Mordacia is still uncertain. The ellipsosome located in the inner segment of M. mordax photoreceptors has a very low absorbance across the entire spectrum, suggesting that it does not have a spectral tuning0filtering function, unlike the yellow short-wavelength absorbing filters within the myoid regions of the photoreceptors in G. australis (Collin et al, 2003a). Given the other retinal adaptations for increasing photon capture in M. mordax, another possible function for the large ellipsosome is to focus light onto the visual pigment within the outer segment.…”

“…Within the Petromyzontidae, Petromyzon marinus (Dickson & Graves, 1979, Lampetra fluviatilis (Öhman, 1971, 1976Holmberg & Öhman, 1976;Holmberg, 1977), L. japonica (Yamada & Ishikawa, 1967;Tonosaki et al, 1989), L. lamottenii (Walls, 1928), Entosphenus sp (Stell, 1972), and Ichthyomyzon unicuspis (S. P. Collin, unpublished data) all appear to contain one type of cone (long) and one type of rod (short) photoreceptor in their retina, although debate still persists. Within the Geotriidae, Geotria australis, the sole member of the family, contains five types of cone photoreceptor based on morphological (Walls, 1942;, spectral (Collin et al, 2003a), and molecular (Collin et al, 2003b;Collin & Trezise, 2004) criteria. The eyes of the southern hemisphere lamprey Mordacia mordax, the subject of this study and one of the two parasitic species in the third family of lampreys, the Mordaciidae, possesses only a single morphological type of photoreceptor with both rod-and cone-like characteristics (Collin & Potter, 2000).…”

Early development of the nervous system of the eutherian <i>Tupaia belangeri</i>

“…"Large globules of mitochondrial origin" (ellipsosomes) with presumed accessory optical functions also have been observed in the Southern Hemisphere lamprey Geotria australis (Collin et al, 2003). This finding is particularly revealing from a phylogenetic perspective, since lampreys and hagfishes represent "the sole survivors of the very early agnathan (jawless) stage in vertebrate evolution" (Hardisty, 1982).…”

“…This finding is particularly revealing from a phylogenetic perspective, since lampreys and hagfishes represent "the sole survivors of the very early agnathan (jawless) stage in vertebrate evolution" (Hardisty, 1982). Interestingly, in Geotria australis, ellipsosomes were exclusively found in medium-wavelength-sensitive cones of nocturnally active upstream migrants, but not in downstream migrants (Collin et al 2003). Hence, ellipsosomes replace the yellow, short wavelength absorbing pigment present in downstream migrants and may help to trap photons.…”