Prolific Origination of Eyes in Cnidaria With Co-Option of Non-Visual Opsins

Picciani, Natasha; Kerlin, Jamie R.; Sierra, Noemie C.; Swafford, Austin D.; Ramirez, M. Desmond; Cannon, Johanna T.; Daly, Marymegan; Oakley, Todd H.

doi:10.2139/ssrn.3155889

Cited by 8 publications

(26 citation statements)

References 57 publications

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“…The organs that fulfill these functions exhibit a variety of morphologies (Serb and Eernisse 2008; Land and Nilsson 2012) and complicated evolutionary histories (e.g., Vopalensky and Kozmik 2009; Henze and Oakley 2015; Picciani et al. 2018). For example, bivalve mollusks have light‐sensitive tissues along the edge of shells that provide nondirectional photoreception (Kennedy 1960; Wiederhold et al.…”

mentioning

confidence: 99%

Hard to get, easy to lose: Evolution of mantle photoreceptor organs in bivalves (Bivalvia, Pteriomorphia)

2020

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Morphologically diverse eyes have evolved numerous times, yet little is known about how eye gain and loss is related to photic environment. The pteriomorphian bivalves (e.g., oysters, scallops, and ark clams), with a remarkable range of photoreceptor organs and ecologies, are a suitable system to investigate the association between eye evolution and ecological shifts. The present phylogenetic framework was based on amino acid sequences from transcriptome datasets and nucleotide sequences of five additional genes. In total, 197 species comprising 22 families from all five pteriomorphian orders were examined, representing the greatest taxonomic sampling to date. Morphological data were acquired for 162 species and lifestyles were compiled from the literature for all 197 species. Photoreceptor organs occur in 11 families and have arisen exclusively in epifaunal lineages, that is, living above the substrate, at least five times independently. Models for trait evolution consistently recovered higher rates of loss over gain. Transitions to crevice‐dwelling habit appear associated with convergent gains of eyespots in epifaunal lineages. Once photoreceptor organs have arisen, multiple losses occurred in lineages that shift to burrowing lifestyles and deep‐sea habitats. The observed patterns suggest that eye evolution in pteriomorphians might have evolved in association with light‐guided behaviors, such as phototaxis, body posture, and alarm responses.

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confidence: 99%

Hard to get, easy to lose: Evolution of mantle photoreceptor organs in bivalves (Bivalvia, Pteriomorphia)

2020

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“…Cnidaria were the first animal organisms to develop nervous systems [38]. Moreover, some Cnidaria in the medusozoan group display complex lens‐containing eyes [39,40]. Since the current analysis suggests that Rax appeared in the common ancestor of Cnidaria and Bilateria, the evolutionary appearance of Rax might underlie the evolution of the eye in this ancestor.…”

Section: Discussionmentioning

confidence: 87%

Origin and evolution of the Rax homeobox gene by comprehensive evolutionary analysis

Kon

Furukawa

2020

FEBS Open Bio

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Rax is one of the key transcription factors crucial for vertebrate eye development. In this study, we conducted comprehensive evolutionary analysis of Rax. We found that Bilateria and Cnidaria possess Rax, but Placozoa, Porifera, and Ctenophora do not, implying that the origin of the Rax gene dates back to the common ancestor of Cnidaria and Bilateria. The results of molecular phylogenetic and synteny analyses on Rax loci between jawed and jawless vertebrates indicate that segmental duplication of the Rax locus occurred in an early common ancestor of jawed vertebrates, resulting in two Rax paralogs in jawed vertebrates, Rax and Rax2. By analyzing 86 mammalian genomes from all four major groups of mammals, we found that at least five independent Rax2 gene loss events occurred in mammals. This study may provide novel insights into the evolution of the eye.

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“…While these discrete origins could be explained by purely random mutations that direct expression of components to evolving eyes, the randomness of this mutation-selection model does not account for some salient features of eye evolution. First, despite evolving many times separately, eyes use functionally similar components (v. Salvini-Plawen and Mayr 1977;Picciani et al 2018) . Second, genetic components of eyes often have dual or ancestral roles in responding to stress.…”

Section: Introductionmentioning

confidence: 99%

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

Swafford

Oakley

2019

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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.

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Prolific Origination of Eyes in Cnidaria With Co-Option of Non-Visual Opsins

Cited by 8 publications

References 57 publications

Hard to get, easy to lose: Evolution of mantle photoreceptor organs in bivalves (Bivalvia, Pteriomorphia)

Hard to get, easy to lose: Evolution of mantle photoreceptor organs in bivalves (Bivalvia, Pteriomorphia)

Origin and evolution of the Rax homeobox gene by comprehensive evolutionary analysis

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

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