The Last Common Ancestor of Most Bilaterian Animals Possessed at Least Nine Opsins

Abstract

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.

Fig. 1.—

There are nine bilaterian opsin paralogs spread among four major eumetazoan opsin paralogs. The four major eumetazoan opsin paralogs are indicated at the top with roman numerals. The nine bilaterian opsin paralogs are indicated with arabic numerals and are color coded to match the corresponding branches. Each opsin clade has been reconciled and collapsed into five major taxonomic groups: chordates, echinoderms, ecdysozoans, lophotrochozoans, and cnidarians. Colored branches indicate the presence of an opsin in at least one species within the major taxonomic group. Light gray dashed branches indicate absence of an opsin paralog from the taxa indicated at the tips. These absences likely represent true losses opsin paralogs. Ultrafast bootstrap (UFBoot) supports from IQ-TREE are given at the nodes they support. All unlabeled nodes had UFBoot supports <95% and were rearranged during tree reconciliation. See supplementary figure S2, Supplementary Material online, for the uncollapsed reconciled tree.

Fig. 2.—

The history of opsins is marked by ancient diversity and subsequent losses of paralogs along different animal lineages. Summary of known opsin complements in major animal phyla. Major subdivisions of metazoans are indicated on the phylogeny as yellow dots with italic labels. Phyla are represented at the tips, except for cnidarians, which are broken down into the two major cnidarian splits. Colored bars with roman numerals indicate opsin paralogs present in the most recent ancestor of eumetazoans. The nine bilaterian opsin paralogs are indicated by slanted colored bars and full opsin names. Filled squares represent presence, empty squares absence of at least one sequence from the opsin paralog group for each phylum listed. Gray Xs mark losses of opsins that are strongly supported, based on absence of that opsin paralog in any genomes from the phylum. Note that no extant phylum included in our analysis seems to have the full complement of bilaterian opsins. The maximum is seven opsin paralogs in both echinoderms and brachiopods. The anthozoan I- canonical visual opsin paralog falls sister to bilaterian orthologs, and is indicated by the light blue bar.

Fig. 3.—

The ancestral mollusc likely had seven opsins from six of the bilaterian paralog groups. Summary of known opsin complements within the molluscs. Colored bars with roman numerals indicate opsin paralogs present in the most recent ancestor of eumetazoans. The nine bilaterian opsin paralogs are indicated by slanted colored bars and full opsin names. Filled squares represent presence, empty squares absence of at least one sequence from the opsin paralog for each genus listed. Gray Xs mark losses of opsins that are strongly supported, based on absence of that opsin paralog in the Octopus bimaculoides genome. The major classes of molluscs are noted with yellow dots and italic labels. Argopecten irradians retinochrome was not included our original analysis, but is present, noted by an asterisk (see supplementary fig. S3, Supplementary Material online, for RGR/retinochrome gene tree that includes this sequence).

Fig. 4.—

Opsin paralog trees for the Gq-opsins and C-opsins, representing the relationships between opsin orthologs by phylum. Each tree shows opsin sequences collapsed by clade. Values below the clade name represent SH-aLRT/aBayes/UFBoots. Only clades with bootstrap supports >75% are shown. The full gene tree can be found in supplementary figure S1, Supplementary Material online.

Fig. 5.—

Opsin paralog trees for the tetraopsins and xenopsins, representing the relationships between opsins by phylum. Each tree shows opsin sequences collapsed by clade. Values below the clade name representSH-aLRT/aBayes/UFBoots. Only clades with bootstrap supports >75% are shown. The full gene tree can be found in supplementary figure S1, Supplementary Material online. Each asterisk “*” on a branch represents a shortening by five branch length units.