Ontogenetic Clues to the Phylogeny of the Visual System

Abstract

The visual system of vertebrates has long presented a puzzle for evolutionary biology: Darwin himself pointed out the difficulties of understanding how such a perfect dioptric apparatus with extra- as well as intraocular muscles, motoneurons, and connections for neuronal analysis could have evolved through stages where this entire system was at best functioning rather differently. Fossil vertebrates have been of very limited help because they either had no eyes or fully developed lateral eyes. Moreover, the relationship of fossil jawless vertebrates to living vertebrates, in particular to hagfish, is largely obscure (Carroll, 1988). The gap in our knowledge of vertebrate lateral eye evolution was addressed in a number of pertinent papers at the turn of the century. The hope at that time was that studies of the organization of the visual system of primitive craniate vertebrates, like hagfish, might provide clues to the ancestral condition of jawed vertebrates. Retzius (1893) was the first to conclude that the eye of hagfish is regressed rather than primitive. Older and more recent suggestions along this line (Franz, 1934; Walls, 1942; Duke-Elder, 1958; Holmberg, 1978; Wicht and Northcutt, 1990) were rooted in the belief that hagfish are modern descendents of fossil jawless vertebrates known to have had large eyes and were supported by the apparent similarities between the hagfish eye and the regressed eyes of some amphibians (Franz, 1934; Wake, 1985) and fish (Franz, 1934; Peters and Peters, 1984). Unfortunately, the differences between the retinae of jawless (Holmberg, 1978) and jawed vertebrates have not been put into an evolutionary context. Consequently, the substantial evidence for evolutionary changes at least in the neural retina as presented here went unrecognized for almost a century.