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New Insights from Genetic Data Sets on the Function and Evolution of Visual Systems: Introduction to a Virtual Symposium in The Biological Bulletin.

Visual systems have long intrigued biologists interested in the function and evolution of complex traits. To understand how eyes function and evolve, it is helpful to identify and characterize their molecular components. For example, one may predict that cells in an animal are likely to be light-sensitive if they express opsin, a type of G-protein-coupled receptor (GPCR) that binds a light-reactive molecule of retinal as a chromophore. If an opsin is from a well-characterized family and its primary sequence is known, we can predict functional aspects of the photoreceptors in which it is expressed, such as the wavelengths of light to which these photoreceptors are most sensitive (Yokoyama, 2000. Prog. Retin. Eye Res. 19: 385-419). The wavelength sensitivities of eyes may then be inferred from the identities and relative expression levels of the opsins expressed in the photoreceptors of their retinas (Carleton and Kocher, 2001. Mol. Biol. Evol. 18: 1540-1550). Thus, genetic data sets help generate important new hypotheses regarding visual function and the evolution of eyes.

By studying molecular components of vision in extant species, we can explore how, when, and in what order the molecular components of a visual system came to be expressed together (Oakley and Speiser, 2015. Annu. Rev. Ecol. Evol. Syst. 46: 237-260). We can also ask questions such as: Do convergent changes in genotype tend to underlie convergent changes in phenotype during the evolution of eyes? And what are the relationships between genotypic and phenotypic complexity in visual systems--for example, to what extent can the number of different opsins expressed in an eye lead to accurate predictions about color vision?

New genetic resources are transforming the field of comparative vision research. New technology for high-throughput genetic sequencing has greatly increased the pace at which we are identifying and characterizing the molecular components of vision. New computational tools for assembling transcrip-tomes de novo (i.e., assembling transcriptomes without the use of a genome as a scaffold) have also been beneficial. These tools have made possible the rapid accumulation of genetic resources for nonmodel organisms that have previously lacked such data but that are well suited for studies of physiology, development, or visual ecology. Combining new genetic resources with emerging methods for genetic manipulation (such as CRISPR/Cas9) allows research to be extended beyond a few model systems, better exploiting organismal diversity and the power of a comparative approach.

In this virtual symposium, several general themes emerge that reflect how new genetic resources are reshaping how we think about the function and evolution of visual systems. First, the sequencing of transcriptomes continues to reveal that light sensitivity in animals extends beyond eyes to tissues such as brains and skin. These extraocular photoreceptors have been difficult to identify in the past because they often lack the morphological specializations--such as expanded surface areas or associations with screening pigments--that characterize photoreceptors found in eyes. For example, Battelle (pp. 3-20) summarizes recent integrative research, indicating that opsin-mediated photosensitivity is distributed widely throughout the central nervous system of the horseshoe crab Limulus. In contrast, Donohue et al. (pp. 58-69) report that mantis shrimp--crustaceans well known for expressing an astonishing diversity of opsins in their eyes--may restrict the distribution of extraocular photoreceptors in their central nervous system to their cerebral ganglion, where they may express as many as four different opsins. As indicated by these two contributions, we continue to discover novel extraocular photoreceptors as we sequence a greater diversity of tissues from a wider range of taxa.

Second, molecular components identified from genetic data sets can help us evaluate the homology of visual systems present in different taxa. In a new analysis of publicly available transcriptomes, Morehouse et al. (pp. 21-38) find that camera-type eyes in spiders develop and function using genes homologous to those employed for similar tasks by the morphologically dissimilar compound eyes found more broadly across arthropods. Conversely, as reported by Bok et al. (pp. 39-57), the morphologically disparate eyes of annelids may not function using homologous molecular components of phototransduction. Bok et al. find that eyes on the fan-like feeding appendages of serpulids, a type of tube-dwelling polychaete worm, detect light using an invertebrate c-opsin. Interestingly, eyes in serpulids may be homologous to those in sabellids, a separate group of fan worms, but do not appear to be homologous to the cephalic eyes of other annelids, which tend to detect light using r-opsins. Taken together, these findings suggest that some eyes may have evolved much more recently than others, with the origin of eyes in fan worms being perhaps a particularly recent event given their limited phylogenetic distribution and molecular dissimilarity to those found in other annelids.

Third, the characterization of opsins from an expanding range of taxa indicates complex patterns of gene diversification and loss in this family of GPCRs, as well as patterns of expression that do not correlate well with physiological complexity. Battelle provides one such example by reviewing evidence that the diversity of opsins expressed in the eyes of Limulus is much higher than was anticipated from the long history of electrophysiological recordings made in this species. A similar situation may exist in copepods: by analyzing new and publicly available transcriptomes from 12 species of these small planktonic crustaceans, Porter et al. (pp. 96-110) find a diversity of opsins, including middle-wavelength-sensitive opsins, pteropsins, peropsins, and Rh7 opsins.

Expanding genetic resources offer new opportunities for those studying the function and evolution of visual systems, but they also present new challenges. One challenge concerns incongruities between the diversities of mRNAs and proteins expressed in a tissue. For example, genetic data sets suggest that eyes in the bay scallop Argopecten express molecular components consistent with phototransduction pathways mediated by the G proteins G[[alpha].sibn.i] or G[[alpha].sub.s] (Wang et al., 2017. Nat. Ecol. Evol. 1: 1-12); however, Kingston et al. (pp. 83-95) do not see patterns of protein expression consistent with these predictions. A second challenge involves predicting functions of novel sequences from nonmodel species. To address this challenge, Faggionato and Serb (pp. 70-82) test a new workflow for discovering novel light-sensitive GPCRs in genetic data sets. Using the bay scallop Argopecten as a test case, they report for the first time the discovery of light-sensitive GPCRs that are not opsins. These new GPCRs appear to bind the same chromophores as opsins (11 -cis and all-trans retinal) but do so using amino acids at different sites in their binding pockets. Thus, they challenge the idea that a comprehensive understanding of the light sensitivity of a tissue can be obtained by characterizing opsin expression alone.

We hope this virtual symposium conveys the message that fundamental discoveries in vision research remain to be made and that we should remain open-minded about the diversity of visual systems at all levels of biological organization.


(1) Department of Biological Sciences, 715 Sumter Street, University of South Carolina, Columbia, South Carolina 29208; and (2) Department of Biology, CB #3280, Coker Hall, University of North Carolina, Chapel Hill, North Carolina 27599

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Author:Speiser, Daniel I.; Kier, William M.
Publication:The Biological Bulletin
Date:Aug 1, 2017
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