A Genetic Perspective on Eye Evolution: Gene Sharing, Convergence and Parallelism

Abstract

Did the diversity of lens-containing eyes evolve from one ancestral eye (monophyletic evolution) or from multiple, independently derived eyes (polyphyletic evolution)? Monophyletic evolution would make diverse eyes homologous (inherited similarities from a common ancestor); polyphyletic evolution would make eyes homoplasious (independently acquired similarities). Historically, anatomical and developmental differences among eyes of different species favored homoplasy; however, recent molecular data indicating that all eyes employ a similar cascade of transcription factors (proteins regulating gene expression) for development have suggested homology. Comparative studies on invertebrates and vertebrates suggest that the use of common networks of developmental transcription factors may be due to parallel evolution, a form of homoplasy by independent recruitments of similar genes and transcriptional networks. Remarkably, the photoreceptors of lens-containing jellyfish eyes have ciliary photoreceptors, like vertebrate photoreceptors, and apparently employ a vertebrate phototransduction system (linked biochemical processes converting light into nervous electrical impulse), consistent with parallel evolution between jellyfish and vertebrate eyes. Finally, the major proteins conferring the lens optical properties - the crystallins - were recruited by a gene-sharing process (the addition of a new gene function without loss of the original function) from various stress proteins and common metabolic enzymes in different species by convergent mutations (derived independently, not related by common ancestry) in their promoters (gene regulatory sequences) leading to high lens expression. Thus, the data indicate that homology or homoplasy of diverse eyes depends upon the level of analysis.