Molecular palaeontology illuminates the evolution of ecdysozoan vision.

James F Fleming,Nicholas W Roberts,Jakob Vinther,Martin Vinther Sørensen,Kazuharu Arakawa,Roberto Guidetti,Tom A Williams,Lorena Rebecchi,Tae-Yoon S Park,Davide Pisani,Reinhardt Møbjerg Kristensen,Mark Blaxter

doi:10.1098/rspb.2018.2180

Abstract

Colour vision is known to have arisen only twice—once in Vertebrata and once within the Ecdysozoa, in Arthropoda. However, the evolutionary history of ecdysozoan vision is unclear. At the molecular level, visual pigments, composed of a chromophore and a protein belonging to the opsin family, have different spectral sensitivities and these mediate colour vision. At the morphological level, ecdysozoan vision is conveyed by eyes of variable levels of complexity; from the simple ocelli observed in the velvet worms (phylum Onychophora) to the marvellously complex eyes of insects, spiders, and crustaceans. Here, we explore the evolution of ecdysozoan vision at both the molecular and morphological level; combining analysis of a large-scale opsin dataset that includes previously unknown ecdysozoan opsins with morphological analyses of key Cambrian fossils with preserved eye structures. We found that while several non-arthropod ecdysozoan lineages have multiple opsins, arthropod multi-opsin vision evolved through a series of gene duplications that were fixed in a period of 35–71 million years (Ma) along the stem arthropod lineage. Our integrative study of the fossil and molecular record of vision indicates that fossils with more complex eyes were likely to have possessed a larger complement of opsin genes.

Highlights

Invertebrates with diverse body plans and ecologies dominated the ecosystems of the Cambrian [1,2,3,4]
Results from ALE [41] and an inspection of our opsin phylogeny clearly indicated that the last common ancestor of the crown arthropods possessed four opsins—the ultraviolet sensitive (UV)/SWS opsin, and the Rh7, MWS, and LWS opsins
Phylogenetic bracketing further implies that trilobites could not have possessed both UV and SWS opsins as these paralogues emerged from a duplication of the UV/SWS opsin that occurred more crownward in the arthropod tree, within Pancrustacea

Summary

Introduction

Invertebrates with diverse body plans and ecologies dominated the ecosystems of the Cambrian [1,2,3,4]. Species from the superphylum Ecdysozoa, including Priapulida ( penis worms) and Arthropoda (e.g. the extant crustaceans, insects, myriapods, and chelicerates) were important constituents of these earliest complex ecosystems. The ability to perceive light and detect visual cues is important for extant animals, allowing them to regulate their circadian rhythms, inform visually guided behaviours such as predation, and communicate through visual signals [5,6]. Given the eye complexity of some Cambrian fossil species, such as Anomalocaris and the trilobites [7], and given that some of these fossils had structural colours [1], it is likely that vision played a role in shaping the Cambrian radiation of animals. License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited

Crustacea

Conclusion

25. Lozano-Fernandez J et al 2016 A molecular