How complexity originates: The evolution of animal eyes

Introduction

How do complex biological traits such as eyes, flight, metabolic pathways, or flowers, originate during evolution? These biological features often appear so functionally integrated and so complicated, that imagining the evolutionary paths to such complexity is sometimes difficult. As such, some anti-evolution creationists maintain that functionally integrated, complex biological systems are “irreducibly complex”, that they cannot originate by evolution, and therefore they must be the product of “intelligent design”. In fact, structurally and functionally complex systems have originated through evolutionary processes. Here, we use eye evolution as a focus for how to implement a research program to gain understanding of the origin of complex traits. This research program first requires defining the trait in question, followed by inferring the timing of past evolutionary events with comparative methods. By understanding when different components came together, we can begin to understand how they came together, and by making inferences about possible functions and environmental context, we can begin to understand why those components stayed together. Eye evolution is particularly amenable to such a research program because we can use optics to predict function from morphology and we can predict gene functions because much is known about the genetic components of eyes and light sensitivity. This approach leads to a narrative on animal eye evolution that, while still incomplete, is already rich and detailed in many facets. We know that a diversity of sometimes disparate eyes have evolved using functional components that interact with light. Many parts of this light interaction hardware kit are used outside of eyes and were recruited into light receptive organs during evolution. But what were these components doing outside of eyes? Here, we propose the hypothesis that several parts of the light-interacting hardware kit were recruited for use in eyes from ancestral roles related to stress response.

Past and present perspectives on origins

Origins have been ignored

Common explanations for the evolution of eyes and other complex traits often involve gradual elaboration. Unfortunately, these explanations effectively ignore origins by taking variation as an implicit assumption. An evolutionary narrative for eyes often begins with a light sensitive patch of cells. That patch evolves to form a deeper and deeper cup, and finally an increasingly more efficient lens evolves within the cup. Such a gradual progression from simple light sensitive patch to complex eye was imagined by Darwin 1859, while he outlined a corollary to his new biological mechanism of natural selection: If complex traits like eyes were produced by natural selection, there should exist a series of functional intermediates between simple patch and complex eye. To show this condition is met, Darwin mentioned functional variation in eye complexity in different species. Later, Salvini-Plawen and Mayr (Salvini-Plawen 1977) illustrated several cases where related species, such as various snails, showed rather finely graded variation between eye-spot and lens-eye. Taking the idea one step farther, (Nilsson 1994) quantified the gradual morphological changes probably necessary to evolve from patch to eye and estimated that the progression can occur rapidly in geological time. Similar gradual-morphological progressions have since been used commonly in textbooks and popular books and videos to help explain how natural selection could have produced an eye. While such a progression is logical and provides a powerful and visual way to imagine the stepwise evolution of complexity, it also has the serious shortcoming of ignoring origins (Oakley 2008). Each gradual step along the progression requires natural selection to act upon variation. However, how this variation originates is not considered: variation is simply assumed. Further, discrete origins are not considered, except again through assuming that the variation simply arose in the past. For example, the origin of light sensitivity in the first place is usually ignored, as is the origin of the cup structure, and the origin of the first lens material. These discrete origins of photosensitivity, a depression, or of lens material are treated no differently than the gradual elaboration of existing structures. Therefore, while not incorrect, using a gradual series of eyes as a model for how evolution proceeds is incomplete, in that it ignores these origins. How did light sensitivity originate? How did lenses originate? Herein we will suggest comparative approaches to these questions.

While the gradual-morphological model of eye evolution is grounded in microevolutionary thinking, macroevolutionary fields like phylogenetics also often ignore origins. By focusing on the distribution of complex traits in different species, phylogeneticists often gain important insights into the timing of evolutionary events. But when they score such traits as simply absent or present, they cannot gain insights into how traits originated because they implicitly assume all components of the trait evolve in concert. For example, armed with a phylogenetic tree, an evolutionist might score species as ‘eyed’ or ‘eyeless’, to infer the number and/or timing of eye gains and losses \cite{Oakley_2002}e.g. Oakley, 2002; Fig. 1. Based on assumptions like parsimony or maximum likelihood, he then may suggest that character states scored in living species can be inferred in common ancestors, leading to inferences of trait history as series of all-or-none gains and losses. Even if the separate components of multi-part systems have different evolutionary histories, scoring complex traits as simply present or absent makes inferring separate histories for components impossible. The inference of all-or-none gains and losses can be said to impose a punctuated mode of evolution, such that all components of a complex trait originate or become extinct simultaneously, but see \cite{Marazzi_2012} for an alternative phylogenetic model.