The opsin gene family encodes key proteins animals use to sense light and has expanded dramatically as it originated early in animal evolution. Understanding the origins of opsin diversity can offer clues to how separate lineages of animals have repurposed different opsin paralogs for different light-detecting functions. However, the more we look for opsins outside of eyes and from additional animal phyla, the more opsins we uncover, suggesting we still do not know the true extent of opsin diversity, nor the ancestry of opsin diversity in animals. To estimate the number of opsin paralogs present in both the last common ancestor of the Nephrozoa (bilaterians excluding Xenoacoelomorpha), and the ancestor of Cnidaria + Bilateria, we reconstructed a reconciled opsin phylogeny using sequences from 14 animal phyla, especially the traditionally poorly-sampled echinoderms and molluscs. Our analysis strongly supports a repertoire of at least nine opsin paralogs in the bilaterian ancestor and at least four opsin paralogs in the last common ancestor of Cnidaria + Bilateria. Thus, the kernels of extant opsin diversity arose much earlier in animal history than previously known. Further, opsins likely duplicated and were lost many times, with different lineages of animals maintaining different repertoires of opsin paralogs. This phylogenetic information can inform hypotheses about the functions of different opsin paralogs and can be used to understand how and when opsins were incorporated into complex traits like eyes and extraocular sensors.
The opsin gene family encodes key proteins animals use to sense light and has expanded dramatically since it originated early in animal evolution. Understanding the origins of opsin diversity can offer clues to how separate lineages of animals have repurposed different opsin paralogs for different lightdetecting functions. However, the more we look for opsins outside of eyes and from additional animal phyla, the more opsins we uncover, suggesting we still do not know the true extent of opsin diversity, nor the ancestry of opsin diversity in animals. To estimate the number of opsin paralogs present in both the last common ancestor of the Nephrozoa (bilaterians excluding Xenoacoelomorpha), and the ancestor of Cnidaria + Bilateria, we reconstructed a reconciled opsin phylogeny using sequences from 14 animal phyla, especially the traditionally poorlysampled echinoderms and molluscs. Our analysis strongly supports a repertoire of at least nine opsin paralogs in the bilaterian ancestor and at least four opsin paralogs in the last common ancestor of Cnidaria + Bilateria. Thus, the kernels of extant opsin diversity arose much earlier in animal history than previously known. Further, opsins likely duplicated and were lost many times, with different lineages of animals maintaining different repertoires of opsin paralogs.This phylogenetic information can inform hypotheses about the functions of different opsin paralogs and be used to understand how and when opsins were incorporated into complex traits like eyes and extraocular sensors.
BackgroundThe eye has evolved across 13 separate lineages of molluscs. Yet, there have been very few studies examining the molecular machinary underlying eye function of this group, which is due, in part, to a lack of genomic resources. The scallop (Bivalvia: Pectinidae) represents a compeling molluscan model to study photoreception due to its morphologically novel and separately evolved mirror-type eye. We sequenced the adult eye transcriptome of two scallop species to: 1) identify the phototransduction pathway components; 2) identify any additional light detection functions; and 3) test the hypothesis that molluscs possess genes not found in other animal lineages.ResultsA total of 3,039 contigs from the bay scallop, Argopecten irradians and 26,395 contigs from the sea scallop, Placopecten magellanicus were produced by 454 sequencing. Targeted BLAST searches and functional annotation using Gene Ontology (GO) terms and KEGG pathways identified transcripts from three light detection systems: two phototransduction pathways and the circadian clock, a previously unrecognized function of the scallop eye. By comparing the scallop transcriptomes to molluscan and non-molluscan genomes, we discovered that a large proportion of the transcripts (7,776 sequences) may be specific to the scallop lineage. Nearly one-third of these contain transmembrane protein domains, suggesting these unannotated transcripts may be sensory receptors.ConclusionsOur data provide the most comprehensive transcriptomic resource currently available from a single molluscan eye type. Candidate genes potentially involved in sensory reception were identified, and are worthy of further investigation. This resource, combined with recent phylogenetic and genomic data, provides a strong foundation for future investigations of the function and evolution of molluscan photosensory systems in this morphologically and taxonomically diverse phylum.
Evolutionary biologists have long been interested in how expansions of the photosensory system might contribute to morphological differentiation of animals. Comparative studies in vertebrate and arthropod lineages have provided considerable insight into how the duplication of opsin, the first gene of the phototransduction pathway, have led to functional differentiation and new ecological opportunities; however, this relationship cannot be examined in many invertebrate groups as we have yet to characterize their opsin content. Scallops (Pectinidae) are a promising molluscan model to study the evolution of opsin and its potential role in speciation. Recently, we discovered a second Gq-coupled, or r-, opsin gene expressed in the eyes of two scallop species. To investigate the evolutionary origin of this opsin, we screened 12 bivalve species from 4 families, representing both mobile and sessile species, with and without eyes. Although only one ortholog was recovered from the genome of the eyeless, immobile oyster, we found both genes to have been retained in 3 families comprising the order Pectinoida. Within this clade, non-mobile species of scallops appear to have lost one gene. Phylogeny-based tests of selection indicate different degrees of purifying selection following duplication. These data, in conjunction with highly divergent gene sequences and ortholog-specific retention, suggest functional differences. Our results are congruent with a Gq-opsin gene duplication in an oyster-Pectinoida ancestor, approximately 470 Mya, and suggest the likelihood of retaining both genes is associated with either the presence of eyes and/or degree of mobility. The identification of two highly divergent Gq-opsin genes in scallops is valuable for future functional investigations and provides a foundation for further study of a morphologically and ecologically diverse clade of bivalves that has been understudied with respect to visual ecology and diversification of opsin.
BackgroundOpsins are the only class of proteins used for light perception in image-forming eyes. Gene duplication and subsequent functional divergence of opsins have played an important role in expanding photoreceptive capabilities of organisms by altering what wavelengths of light are absorbed by photoreceptors (spectral tuning). However, new opsin copies may also acquire novel function or subdivide ancestral functions through changes to temporal, spatial or the level of gene expression. Here, we test how opsin gene copies diversify in function and evolutionary fate by characterizing four rhabdomeric (Gq-protein coupled) opsins in the scallop, Argopecten irradians, identified from tissue-specific transcriptomes.ResultsUnder a phylogenetic analysis, we recovered a pattern consistent with two rounds of duplication that generated the genetic diversity of scallop Gq-opsins. We found strong support for differential expression of paralogous Gq-opsins across ocular and extra-ocular photosensitive tissues, suggesting that scallop Gq-opsins are used in different biological contexts due to molecular alternations outside and within the protein-coding regions. Finally, we used available protein models to predict which amino acid residues interact with the light-absorbing chromophore. Variation in these residues suggests that the four Gq-opsin paralogs absorb different wavelengths of light.ConclusionsOur results uncover novel genetic and functional diversity in the light-sensing structures of the scallop, demonstrating the complicated nature of Gq-opsin diversification after gene duplication. Our results highlight a change in the nearly ubiquitous shadow response in molluscs to a narrowed functional specificity for visual processes in the eyed scallop. Our findings provide a starting point to study how gene duplication may coincide with eye evolution, and more specifically, different ways neofunctionalization of Gq-opsins may occur.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0823-9) contains supplementary material, which is available to authorized users.
Scallops (Pectinidae) are one of the most diverse families of bivalves and have been a model system in evolutionary biology. However, in order to understand phenotypic evolution, the Pectinidae needs to be placed in a deeper phylogenetic framework within the superfamily Pectinoidea. We reconstructed a molecular phylogeny for 60 species from four of the five extant families within the Pectinoidea using a five gene dataset (12S, 16S, 18S, 28S rRNAs and histone H3). Our analyses give consistent support for the non-monophyly of the Propeamussiidae, with a subset of species as the sister group to the Pectinidae, the Propeamussiidae type species as sister to the Spondylidae, and the majority of propeamussiid taxa sister to the Spondylidae + Pr. dalli. This topology represents a previously undescribed relationship of pectinoidean families. Our results suggest a single origin for eyes within the superfamily and likely multiple instances of loss for these characters. However, it is now evident that reconstructing the evolutionary relationships of Pectinoidea will require a more comprehensive taxonomic sampling of the Propeamussiidae sensu lato.
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