Disparate compound eyes of Cambrian radiodonts reveal their developmental growth mode and diverse visual ecology

Paterson, John R.; Edgecombe, Gregory D.; García‐Bellido, Diego C.

doi:10.1126/sciadv.abc6721

Cited by 25 publications

(28 citation statements)

References 61 publications

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“…For instance, the neural architectures seen in Cambrian panarthropods (Ma et al 2012; Tanaka et al 2013; Cong et al 2014; Strausfeld 2015) are quite conserved and similar in complexity to those in the present. Likewise, Ma et al (2012: p. 258) characterize compound eyes in the Cambrian as being “in size and resolution, equal to those of modern insects and malacostracans.” Such inference about Cambrian compound eyes is seen, for instance, from Paterson et al's (2011, 2020) finding that the stem-arthropod Anomalocaris compared well to most living arthropods in eye size, high ommatidial lens count per eye, and low interommatidial angles, all factors that correlate with visual acuity in the present. These claims would imply that modern levels of cognition and sensory acuity were achieved exceptionally early for arthropods.…”

Section: Discussionsupporting

confidence: 64%

The Phanerozoic aftermath of the Cambrian information revolution: sensory and cognitive complexity in marine faunas

Hsieh¹,

Plotnick²,

Bush³

2022

Paleobiology

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The Cambrian information revolution describes how biotically driven increases in signals, sensory abilities, behavioral interactions, and landscape spatial complexity drove a rapid increase in animal cognition concurrent with the Cambrian radiation. Here, we compare cognitive complexity in Cambrian and post-Cambrian marine ecosystems, documenting changes in animal cognition after the initial Cambrian increase. In a comparison of Cambrian and post-Cambrian Lagerstätten, we find no strong trend in the proportion of genera possessing two types of macroscopic sense organs (eyes and chemoreceptive organs such as antennae, feelers, or nostrils). There is also no trend in general nervous system complexity. These results suggest that sophisticated information processing was already common in early Phanerozoic ecosystems, comparable with behavioral evidence from the trace fossil record. Most taxa capable of complex information processing in Cambrian ecosystems were panarthropods, whereas mollusks and chordates made up larger proportions afterward. In both the Cambrian and the present day, ecological occupation of diverse habitat tiers and feeding modes is possible with even simple nervous systems, but ecological lifestyles requiring rapid, regular movement are almost exclusively associated within brain-bearing taxa, suggesting a connection with fast information-processing abilities and bodily responses. The overall rise in cognitive sophistication in the Cambrian was likely a unique event in the history of life, although some lineages subsequently developed more elaborate sensory systems and/or larger brains.

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Section: Discussionsupporting

confidence: 64%

The Phanerozoic aftermath of the Cambrian information revolution: sensory and cognitive complexity in marine faunas

Hsieh¹,

Plotnick²,

Bush³

2022

Paleobiology

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“…Indeed, in hemimetabolous insects, compound eyes grow by adding new units peripherally rather than between units that have already formed (Friedrich, 2008). Even in fossil radiodonts, compound eye units were added at the periphery (Paterson et al, 2020). Finally, consistent with these expectations, it was recently demonstrated that the eyes of tiny juvenile jumping spiders have approximately the same number of PRs as those of their much larger adult counterparts (Goté et al, 2019).…”

Section: The Apoptosis Rate Of Remaining Cells Molds the Final Eye La...mentioning

confidence: 75%

EyeVolve, a modular PYTHON based model for simulating developmental eye type diversification

Lavin

Rathore

Bauer

et al. 2022

Front. Cell Dev. Biol.

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Vision is among the oldest and arguably most important sensory modalities for animals to interact with their external environment. Although many different eye types exist within the animal kingdom, mounting evidence indicates that the genetic networks required for visual system formation and function are relatively well conserved between species. This raises the question as to how common developmental programs are modified in functionally different eye types. Here, we approached this issue through EyeVolve, an open-source PYTHON-based model that recapitulates eye development based on developmental principles originally identified in Drosophila melanogaster. Proof-of-principle experiments showed that this program’s animated timeline successfully simulates early eye tissue expansion, neurogenesis, and pigment cell formation, sequentially transitioning from a disorganized pool of progenitor cells to a highly organized lattice of photoreceptor clusters wrapped with support cells. Further, tweaking just five parameters (precursor pool size, founder cell distance and placement from edge, photoreceptor subtype number, and cell death decisions) predicted a multitude of visual system layouts, reminiscent of the varied eye types found in larval and adult arthropods. This suggests that there are universal underlying mechanisms that can explain much of the existing arthropod eye diversity. Thus, EyeVolve sheds light on common principles of eye development and provides a new computational system for generating specific testable predictions about how development gives rise to diverse visual systems from a commonly specified neuroepithelial ground plan.

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“…Another important trait associated with the appearance of radiodontans is the presence of well‐developed compound eyes, which in these taxa are stalked (Paterson et al ., 2011; but see Paterson, Edgecombe & García‐Bellido, 2020), whereas lobopodians only possess simple ocelli (Ma et al ., 2012a), when present (Fig. 2).…”

Section: Assembly Of the Arthropod Body Planmentioning

confidence: 99%

The origin and early evolution of arthropods

Aria

2022

Biological Reviews

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The rise of arthropods is a decisive event in the history of life. Likely the first animals to have established themselves on land and in the air, arthropods have pervaded nearly all ecosystems and have become pillars of the planet's ecological networks. Forerunners of this saga, exceptionally well-preserved Palaeozoic fossils recently discovered or re-discovered using new approaches and techniques have elucidated the precocious appearance of extant lineages at the onset of the Cambrian explosion, and pointed to the critical role of the plankton and hard integuments in early arthropod diversification. The notion put forward at the beginning of the century that the acquisition of extant arthropod characters was stepwise and represented by the majority of Cambrian fossil taxa is being rewritten. Although some key traits leading to Euarthropoda are indeed well documented along a diversified phylogenetic stem, this stem led to several speciose and ecologically diverse radiations leaving descendants late into the Palaeozoic, and a large part, if not all of the Cambrian euarthropods can now be placed on either of the two extant lineages: Mandibulata and Chelicerata. These new observations and discoveries have altered our view on the nature and timing of the Cambrian explosion and clarified diagnostic characters at the origin of extant arthropods, but also raised new questions, especially with respect to cephalic plasticity. There is now strong evidence that early arthropods shared a homologous frontalmost appendage, coined here the cheira, which likely evolved into antennules and chelicerae, but other aspects, such as brain and labrum evolution, are still subject to active debate. The early evolution of panarthropods was generally driven by increased mastication and predation efficiency and sophistication, but a wealth of recent studies have also highlighted the prevalent role of suspension-feeding, for which early panarthropods developed their own adaptive feedback through both specialized appendages and the diversification of small, morphologically differentiated larvae. In a context of general integumental differentiation and hardening across Cambrian metazoans, arthrodization of body and limbs notably prompted two diverging strategies of basipod differentiation, which arguably became founding criteria in the divergence of total-groups Mandibulata and Chelicerata. The kinship of trilobites and their relatives remains a source of disagreement, but a recent topological solution, termed the 'deep split', could embed Artiopoda as sister taxa to chelicerates and constitute definitive support for Arachnomorpha. Although Cambrian fossils have been critical to all these findings, data of exceptional quality have also been accumulating from other Palaeozoic Konservat-Lagerstätten, and a better integration of this information promises a much more complete and elaborate picture of early arthropod evolution in the near future. From the broader perspective of a total-evidence approach to the understanding of life's history, and ...

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Disparate compound eyes of Cambrian radiodonts reveal their developmental growth mode and diverse visual ecology

Cited by 25 publications

References 61 publications

The Phanerozoic aftermath of the Cambrian information revolution: sensory and cognitive complexity in marine faunas

The Phanerozoic aftermath of the Cambrian information revolution: sensory and cognitive complexity in marine faunas

EyeVolve, a modular PYTHON based model for simulating developmental eye type diversification

The origin and early evolution of arthropods

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