The Ocular Morphology of the Southern Hemisphere Lamprey Geotria australis Gray, with Special Reference to Optical Specialisations and the Characterisation and Phylogeny of Photoreceptor Types

Abstract

This paper describes the ocular morphology of young adults of the southern hemisphere lamprey Geotria australis, the sole representative of the Geotriidae, and makes comparisons with those of holarctic lampreys (Petromyzontidae). As previously reported for the holarctic lamprey Ichthyomyzon unicuspis [Collin and Fritzsch, 1993], the lens of G. australis is non-spherical and possesses a cone-shaped posterior that may be capable of mediating variable focus. The avascular retina of G. australis is well differentiated, containing three retinal ganglion cell populations, three layers of horizontal cells and three photoreceptor types. In contrast to petromyzontids that contain only two photoreceptor types (short and long), G. australis possesses one rod-like (R1) and two cone-like (C1 and C2) photoreceptors. Although the rod-like receptor in G. australis may be homologous with the short receptors of holarctic lampreys, the two cone-like receptors have morphological characteristics that differ markedly from those of the long receptors of their holarctic counterparts. The features which distinguish the two cone-like receptors from those of the long receptor type in holarctic lampreys are the characteristics of the mitochondria and the presence of large amounts of two different types of stored secretory material in the endoplasmic reticulum of the myoid (refractile bodies). The endoplasmic reticulum of each receptor type has a different shape and staining profile and is polymorphic, each showing a continuum of distension. It is proposed that the presence of two cone-like photoreceptors with different characteristics would increase the spectral range of G. australis and thus be of value during the parasitic phase, when this lamprey lives in the surface marine waters. The irideal flap, present in G. australis but not petromyzontids, would assist in reducing intraocular flare during life in surface waters. The results of this study, which are discussed in the context of the proposed evolution of lampreys, emphasise that it is important to take into account the characteristics of the eyes of southern hemisphere lampreys when making generalizations about the eyes of lampreys as a whole.

The evolution of early vertebrate photoreceptors

“…These findings were later refuted by several authors who identified conelike receptors in the eyes of cyclostomes, i.e. lampreys (Ö hman 1971;Dickson & Graves 1979;Govardovskii & Lychakov 1984;Tonosaki et al 1989;Collin et al 1999;Collin & Trezise 2004), but the characterization and distinction of rods and cones in the early vertebrates is not at all clear and has been the subject of great debate for over 150 years (Crescitelli 1972).…”

Multiple cone visual pigments and the potential for trichromatic colour vision in two species of elasmobranch

“…For light microscopy, enucleated eyes were immersion fixed in 4% paraformaldehyde in 0. cacodylate buffer (pH·7.4) and embedded in araldite before being sectioned on an LKB rotary ultramicrotome (Collin et al, 1999). Ultra-thin sections were stained with lead citrate and uranyl acetate, and examined on either a Phillips 410 or a Phillips CM10 transmission electron microscope set at 80·kV (Phillips Inc., Eindhoven, The Netherlands).…”

Early evolution of vertebrate photoreception: lessons from lampreys and lungfishes

“…In both downstream and upstream migrant phases of the adult lifecycle of the pouched lamprey, Geotria australis, the sole representative of the Geotriidae family of southern hemisphere lampreys, five types of photoreceptor have been identified (Collin et al 1999(Collin et al , 2003aCollin & Trezise 2004;Fig. 2B).…”

“…However, an intracellular yellow/orange photostable pigment is present in the myoid and ellipsoidal regions of at least three of the five photoreceptor types in the southern hemisphere lamprey G. australis (Collin et al 1999;Collin & Trezise 2004;Figs 2B,3A,B). This pigment, which is also retained within one of the cone photoreceptor types in N. forsteri (Bailes et al 2006;Figs 2D, 3C), acts as a spectral filter, which absorbs wavelengths below approximately 550 nm (Collin et al 2003a).…”

“…Two major lines of new evidence now suggest that this ancestral visual system relied on a complex color vision, which evolved at least 540 mA. This is based on the presence of five types of cone-like photoreceptors in the southern hemisphere lamprey G. australis (Collin et al 1999;Collin & Trezise 2004) with the retention of four cone types with different colored oil droplets/inclusions in the Australian lungfish, N. forsteri (Robinson 1994;Bailes et al 2006Bailes et al , 2007. Further work is needed on the remaining "primitive" groups; the Chondrichthyes (sharks, skates and rays, but see Hart et al 2005Hart et al , 2004Theiss et al 2007); and the non-Actinopterygii (early ray-finned fishes).…”