How complexity originates: The evolution of animal eyes

Abstract

Learning how complex traits like eyes originate is fundamental for understanding evolution. Here, we first sketch historical perspectives on trait origins and argue that new technologies offer key new insights. Next, we articulate four open questions about trait origins. To address them, we define a research program to break complex traits into components and study the individual evolutionary histories of those parts. By doing so, we can learn when the parts came together and perhaps understand why they stayed together. We apply the approach to five structural innovations critical for complex eyes, reviewing the history of the parts of each of those innovations. Photoreceptors evolved within animals by bricolage, recombining genes that originated far earlier. Multiple genes used in eyes today had ancestral roles in stress responses. We hypothesize that photo-stress could have increased the chance those genes were expressed together in places on animals where light was abundant.

The non‐visual opsins: eighteen in the ancestor of vertebrates, astonishing increase in ray‐finned fish, and loss in amniotes

“…Consistent with this hypothesis, Blanco‐Vive, Aliaga‐Guerrero, Canavate, Munoz‐Cueto, and Sanchez‐Vazquez () showed that the amount and wavelength of light influenced hatching, growth, and development rate in Senegal sole ( Sola senegalensis ) and Villamizar, Vera, Foulkes, and Sanchez‐Vazquez () found that the amount and the wavelength of light influenced the onset of locomotor activity in developing zebrafish. Non‐visual opsins might also induce a protective response to photo‐oxidative stress and DNA damage caused by exposure to light (Oakley & Speiser, ). Larval amphibians and fish are particularly susceptible because they are translucent/transparent.…”

On the Origin of Complex Adaptive Traits: Progress Since the Darwin Versus Mivart Debate

“…3; Suzuki et al, 2014). From a similar standpoint, the importance of such a component-based approach was discussed by taking the evolution of animal eyes as an example (Oakley and Speiser, 2015).…”

How exaptations facilitated photosensory evolution: Seeing the light by accident

“…One of the newest debates -and the one most pertinent to vision in humans -is whether the opsins of animals were exapted from melatonin receptors [11,15,16]. Despite the intriguing possibility that a hormone receptor gained the ability sense light, we will not discuss this here, as opsin evolution has been thoroughly reviewed elsewhere [10,17]. Microbial photoreceptors, meanwhile, are rarely included in reviews of eye evolution, yet they have much to teach us about photosensory evolution.…”

“…Since the elucidation of lens crystallins, the conceptual usefulness of exaptation has broadened further, and is now a consideration in even more ancient features of DOI 10.1002/bies.201600266 photoreception [8]. This includes the Pax-6 master control genes that initiate eye development [9], as well as diverse phototransduction pathways in animals [10], and even the origins of opsins in animals [11]. Here we expand on this theme, mainly drawing on discoveries in microbial eukaryotes (protists), such as phytoplankton and unicellular fungi.…”