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 lenscontaining 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.

The Evolution of Complex Organs

“…At the molecular level, it is becoming increasingly recognized that the same protein can carry out more than one function, though it can sometimes be difficult to determine which, if either, was the sole original function. In this sense, a descriptor other than "exaptation" or "co-option" is used in reference to the existence of multifunctional proteins: "gene sharing" (Piatigorsky 2007(Piatigorsky , 2008.…”

“…4. Others argue for a more restrictive definition under which an eye is an organ that can produce an image, however crude, and not simply detect light (e.g., Land and Nilsson 2002;Piatigorsky 2008;Serb and Eernisse 2008). Even under this stricter definition, there are at least eight different types of eyes, 5 prominent examples of which variously employ cups, pinholes, camera-type lenses, arrays of lenses, concave mirrors, or telescope-like arrangements for image formation (Land and Fernald 1992;Land and Nilsson 2002;Serb and Eernisse 2008).…”

Homoplasy, a Moving Target

“…We may have to take it at face value from molecular biology that this gene is indeed the same thing, and for the purposes of making progress in Evo-devo research we might as well accept its homology because we have no reason (at present) not to do so. What has been called "deep homology" is the recognition that structures such as eyes of vertebrates and cephalopods (Piatagorsky 2008) and appendages of arthropods and vertebrates (Shubin et al 2009) share some developmental genetic systems in common, which are derived from common ancestors and deployed in different organismal and evolutionary contexts. In this sense, the clearly homoplastic organs (because ancestors of both groups lacked fully formed eyes, as well as multipart appendages) share some remotely similar features due to their extremely ancient common ancestry.…”

Introduction

“…The peer-reviewed papers presented in this issue by experts in their fields provide a further introduction to this information, most of which is, unfortunately, unknown to nonspecialists. In this regard, Oakley and Pankey (2008) and Piatigorsky (2008) provide discussions of the genetic and molecular components of eye evolution: a former "black box" whose contents are now being well illuminated. Regarding vertebrate eyes, Lamb et al (2008) review information based on comparisons of modern species, while Young (2008) discusses the eyes of early fossil fishes.…”