A morphological basis for path dependent evolution of visual systems

Varney, Rebecca M.; Speiser, Daniel I.; Cannon, Johanna T.; Aguilar, Morris A; Eernissee, Douglas J.; Oakley, Todd H.

doi:10.1101/2022.12.20.520810

“…By producing enzymes, structural proteins, regulatory factors, and other molecular components, these genes govern the formation and development of biominerals, such as skeletons, which evolved convergently many times (Murdock 2020). Similarly, a light interaction toolkit includes animal genes involved in the biochemistry, physiology, and development of light-interacting structures such as eyes and light-producing photophores, which also evolved convergently many times (v. Salvini-Plawen and Mayr 1977;Picciani et al 2018;Lau and Oakley 2021;Varney et al 2024).…”

Section: Defining and Operationalizing Genetic Toolkitsmentioning

confidence: 99%

Building, Maintaining, and (Re-)Deploying Genetic Toolkits during Convergent Evolution

Oakley

2024

Preprint

1

0

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A surprising insight from the advent of genomic sequencing was that many genes are deeply conserved during evolution. With a particular focus on genes that interact with light in animals, I explore the metaphor of genetic toolkits, which can be operationalized as lists of genes involved in a trait of interest. A fascinating observation is that genes of a toolkit are often used again and again during convergent evolution, sometimes across vast phylogenetic distances. Such a pattern in the evolution of toolkits requires three different stages: origin, maintenance, and redeployment of the genes. The functional origins of toolkit genes might often be rooted in interactions with external environments. The origins of light interacting genes in particular may be tied to ancient responses to photo-oxidative stress, inspiring questions about the extent to which the evolution of other toolkits were also impacted by stress. Maintenance of genetic toolkits over long evolutionary timescales requires gene multifunctionality to prevent gene loss when a trait of interest is absent. Finally, the deployment of toolkit genes in convergently evolved traits like eyes sometimes involves the repeated use of similar, ancient genes but other times involves different genes specific to each convergent origin. How often a particular gene family is used time and again for the same function may depend on how many possible biological solutions are available. When few solutions exist and are maintained, evolution is constrained to use the same genes over and over. However, when many different solutions are possible, the innovative possibilities of evolution are often on display. Therefore, a focus on genetic toolkits highlights the combination of legacy plus innovation that drives the evolution of biological diversity.

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“…By producing enzymes, structural proteins, regulatory factors, and other molecular components, these genes govern the formation and development of biominerals, such as skeletons, which evolved convergently many times (Murdock 2020). Similarly, a "light interaction toolkit" includes animal genes involved in the biochemistry, physiology, and development of light-interacting structures such as eyes, which evolved convergently many times (v. Salvini-Plawen and Mayr 1977; Picciani et al 2018;Varney et al 2024).…”

Section: Defining and Operationalizing Genetic Toolkitsmentioning

confidence: 99%

Building, Maintaining, and (Re-)Deploying Genetic Toolkits during Convergent Evolution

Oakley

2024

Preprint

1

0

View full text Add to dashboard Cite

A surprising insight from the advent of genomic sequencing was that many genes are deeply conserved during evolution. With a particular focus on genes that interact with light in animals, I explore the metaphor of genetic toolkits, which can be operationalized as lists of genes involved in a trait of interest. A fascinating observation is that genes of a toolkit are often used again and again during convergent evolution, sometimes across vast phylogenetic distances. Such a pattern in the evolution of toolkits requires three different stages: origin, maintenance, and redeployment of the genes. The functional origins of toolkit genes might often be rooted in interactions with external environments. The origins of light interacting genes in particular may be tied to ancient responses to photo-oxidative stress, inspiring questions about the extent to which the evolution of other toolkits were also impacted by stress. Maintenance of genetic toolkits over long evolutionary timescales requires gene multifunctionality to prevent gene loss when a trait of interest is absent. Finally, the deployment of toolkit genes in convergently evolved traits like eyes sometimes involves the repeated use of similar, ancient genes but other times involves different genes specific to each convergent origin. How often a particular gene family is used time and again for the same function may depend on how many possible biological solutions are available. When few solutions exist and are maintained, evolution is constrained to use the same genes over and over. However, when many different solutions are possible, the innovative possibilities of evolution are often on display. Therefore, a focus on genetic toolkits highlights the combination of legacy plus innovation that drives the evolution of biological diversity.

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“…We reasoned that See-Star could also be applied to study structures that closely underlie or pass through shells, such as the sensory aesthetes of chitons, which are neural sensory organs that reside in hollow channels within the valves (shell plates) [29][30][31]. While heavily pigmented and calcified in life, chitons processed with See-Star were rendered nearly transparent (Fig.…”

Section: See-star Is Compatible With Immunohistochemistry In Diverse ...mentioning

confidence: 99%

See-Star: a versatile hydrogel-based protocol for clearing large, opaque and calcified marine invertebrates

Clarke,

Formery,

Lowe

2024

EvoDevo

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0

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Studies of morphology and developmental patterning in adult stages of many invertebrates are hindered by opaque structures, such as shells, skeletal elements, and pigment granules that block or refract light and necessitate sectioning for observation of internal features. An inherent challenge in studies relying on surgical approaches is that cutting tissue is semi-destructive, and delicate structures, such as axonal processes within neural networks, are computationally challenging to reconstruct once disrupted. To address this problem, we developed See-Star, a hydrogel-based tissue clearing protocol to render the bodies of opaque and calcified invertebrates optically transparent while preserving their anatomy in an unperturbed state, facilitating molecular labeling and observation of intact organ systems. The resulting protocol can clear large (> 1 cm3) specimens to enable deep-tissue imaging, and is compatible with molecular techniques, such as immunohistochemistry and in situ hybridization to visualize protein and mRNA localization. To test the utility of this method, we performed a whole-mount imaging study of intact nervous systems in juvenile echinoderms and molluscs and demonstrate that See-Star allows for comparative studies to be extended far into development, facilitating insights into the anatomy of juveniles and adults that are usually not amenable to whole-mount imaging.

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A morphological basis for path dependent evolution of visual systems

Cited by 3 publications

References 75 publications

Building, Maintaining, and (Re-)Deploying Genetic Toolkits during Convergent Evolution

Building, Maintaining, and (Re-)Deploying Genetic Toolkits during Convergent Evolution

Building, Maintaining, and (Re-)Deploying Genetic Toolkits during Convergent Evolution

See-Star: a versatile hydrogel-based protocol for clearing large, opaque and calcified marine invertebrates

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