Light-Induced Stress as a Primary Evolutionary Driver of Eye Origins

Abstract

Eyes are quintessential complex traits and our understanding of their evolution guides understanding of trait evolution in general. A long-standing account of eye evolution argues natural selection favors morphological variations that allow increased functionality for sensing light (Darwin 1859; v. Salvini-Plawen and Mayr 1977; Nilsson and Pelger 1994; Nilsson 2013). While certainly true in part, this focus on visual performance does not entirely explain why diffuse photosensitivity persists even after eyes evolve, or why eyes evolved many times, each time using similar building blocks. Here we briefly review a vast literature indicating most genetic components of eyes historically responded to stress caused directly by light, including UV damage of DNA, oxidative stress, and production of aldehydes. We propose light-induced stress had a direct and prominent role in the evolution of eyes by bringing together genes to repair and prevent damage from light-stress, both before and during the evolution of eyes themselves. Stress-repair and stress-prevention genes were perhaps originally deployed as plastic responses to light and/or as beneficial mutations genetically driving expression where light was prominent. These stress-response genes sense, shield, and refract light but only under UV exposure. Once under regulatory-genetic control, they could be expressed before UV stress appeared, evolve as a single unit, and be influenced by natural selection to increase functionality for sensing light, ultimately leading to complex eyes and behaviors. Recognizing the potentially prominent role of stress in eye evolution invites discussions of plasticity and assimilation and provides a hypothesis for why similar genes are repeatedly used in convergent eyes. Broadening the drivers of eye evolution encourages consideration of multi-faceted mechanisms of plasticity/assimilation and mutation/selection for complex novelties and innovations in general.

Co‐option of stress mechanisms in the origin of evolutionary novelties

“…Thus, the capacity of cells exposed to UV radiation to monitor retinal levels and coordinate the stress response is a consequence of co‐option that also affords an evolutionary opportunity to evolve photoreception and thus photoreceptor cells. More generally, there is a repeated pattern of essential physiological functions of the eye being molecularly realized by mechanisms that show strong evidence of homology to stress response pathways, which supports a SIEI model that derives the building blocks of eye development and function from preexisting stress mechanisms (Swafford and Oakley 2019).…”

“…However, these accounts are based on the availability of potentially beneficial variants that facilitate adaptation. “Attempting to justify the origin of eyes based solely on selection for improved visual acuity creates circular reasoning, leaving no obvious evolutionary starting point for eyes or parts of eyes to independently evolve” (Swafford and Oakley 2019, p. 746). Oakley and collaborators have developed and documented a complementary narrative whereby the main building blocks of complex eyes originated from elements of the light and UV stress response (Oakley and Speiser 2015; Swafford and Oakley 2019) (Fig.…”

“…1 from Umen 2020 reproduced with permission); (B) evolution of slime mold multicellularity (fig. 1 from Schaap 2021 reproduced with permission); (C) stepwise elaboration of the eye according to Swafford and Oakley (2019) (reproduced with permission). Each additional structure of the eye is derived from a stress‐related compensation: 1, Photoreceptors, from retinal sequestering opsins; 2, Pigment cells; 3, Lens cells from chaperone production; 4, Cilia in photoreceptors (for detailed discussion, see Swafford and Oakley 2019).…”