Opening the “Black Box”: The Genetic and Biochemical Basis of Eye Evolution

Abstract

Eyes provide a rich narrative for understanding evolution, having attracted the attention of preeminent scientists and communicators alike. Until recently, this narrative has focused primarily on the evolution of eye structure and far less on biochemistry or genetics. Although eye biochemistry was once likened to an unknown "black box;" the flood of discoveries in biochemistry is now allowing an increasingly detailed understanding of the processes involved in vision. As a result, evolutionary comparative ("tree-thinking") analyses that use these data currently allow a new and still unfolding narrative, both richer in detail and more comprehensive in scope. Rather than toppling evolutionary theory by finding irreducibly complex molecular machines, eye evolution provides detailed accounts of how natural processes tinker with existing genetic components, duplicating and recombining them, to yield complex, intricate, and highly functional eyes. Understanding the new biochemical narrative is critical for researchers and teachers alike, in order to answer antievolutionist claims, and to provide an up-to-date account of the state of knowledge on the subject of eye evolution.Keywords Evolution . Phototransduction . Vision . Eyes . Phylogeny . Novelty . ComplexityThe evolutionary history of eyes is one of the most intriguing and often-told stories in biology. It is a topic researched and discussed by members of the pantheon of evolutionists, including Darwin (1859), Salvini-Plawen and Mayr (1977), Gould (1994), andDawkins (1996). The commonly told story is familiar and has not changed much since Darwin first proposed it: A light-sensitive nerve gradually changes over evolutionary time, adding complexity across the generations. To Darwin's sketch, Salvini-Plawen and Mayr (1977) added detail, and Nilsson and Pelger (1994) tested the temporal component. The ancient canon of gradual evolution is certainly valuable for demonstrating that some assumptions are met for the hypothesis that natural selection generates complexity, serving as a colorful and graphical example (Dawkins 1996). However, this account-if taken too far-can easily be criticized, as demonstrated, for example, by proponents of Intelligent Design (ID; Behe 1996) who point out that the Darwinian canon ignores complexity at the molecular level. The structure of this article is first to briefly present the "gradual morphological" account of the evolution of eye form and to describe how this account relates to understanding evolution by natural selection. Section II will point out two primary limitations of this "gradual morphological" model, including one highlighted by ID proponents. Third, the paper will present molecular and biochemical details describing how phototransduction (the cascade of signaling events that generate a nervous impulse in response to light) and complex lenses evolved. These two case studies provide specific details about how eyes evolved. The processes elucidated, such as duplication and co-option (the use of existing components ...

The Evolution of Complex Organs

“…Those that occur in animals are divided into seven subfamilies, all of which appear to have originated before the split between the protostomes (most invertebrates) and deuterostomes (chordates and relatives including echinoderms) (Terakita 2005;Larusso et al 2008). The extraordinary diversity of opsin molecules is likely a product of extensive gene duplication and subsequent divergence (Arendt 2003;Plachetzki and Oakley 2007;Oakley and Pankey 2008). Importantly, the duplication of opsin genes and their divergence in becoming reactive to different wavelengths of light forms the basis of color vision (e.g., Dulai et al 1999;Spady et al 2006;Briscoe 2008;Gerl and Morris 2008).…”

“…Note that these images are not drawn to the same scale (Nautilus eyes are about 10 mm across whereas the others are about 1 mm). From Land and Nilsson (2002), based on drawings by Hesse (1908 (2002), Arendt (2003), Gehring (2004Gehring ( , 2005, Terakita (2005), Plachetzki et al (2005Plachetzki et al ( , 2007, Bowmaker and Hunt (2006), Purschke et al (2006), Santillo et al (2006), Lamb et al (2007), Kawamura and Tachibanaki (2008), and Oakley and Pankey (2008). This hypothesis is based on several independent lines of evidence, including analyses of genes and proteins, comparisons of living species with differing degrees of eye complexity, and information regarding the development of eyes in embryonic vertebrates.…”

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.…”

Misconceptions About the Evolution of Complexity

“…Readers interested in a detailed discussion of the evolution of complex features should consult Gregory (2008), and those seeking a comprehensive overview of the state of our current knowledge of eye evolution should consult Lamb et al (2007Lamb et al ( , 2008, Buschbeck and Friedrich (2008), Cronin and Porter (2008), Oakley and Pankey (2008), Piatigorsky (2008), and Serb and Eernisse (2008).…”