Analysis of the opsin repertoire in the tardigrade Hypsibius dujardini provides insights into the evolution of opsin genes in panarthropoda

Abstract

Screening of a deeply sequenced transcriptome using Illumina sequencing as well as the genome of the tardigrade Hypsibius dujardini revealed a set of five opsin genes. To clarify the phylogenetic position of these genes and to elucidate the evolutionary history of opsins in Panarthropoda (Onychophora + Tardigrada + Arthropoda), we reconstructed the phylogeny of broadly sampled metazoan opsin genes using maximum likelihood and Bayesian inference methods in conjunction with carefully selected substitution models. According to our findings, the opsin repertoire of H. dujardini comprises representatives of all three major bilaterian opsin clades, including one r-opsin, three c-opsins, and a Group 4 opsin (neuropsin/opsin-5). The identification of the tardigrade ortholog of neuropsin/opsin-5 is the first record of this opsin type in a protostome, but our screening of available metazoan genomes revealed that it is also present in other protostomes. Our opsin phylogeny further suggests that two r-opsins, including an "arthropsin," were present in the last common ancestor of Panarthropoda. Although both r-opsin lineages were retained in Onychophora and Arthropoda, the arthropsin was lost in Tardigrada. The single (most likely visual) r-opsin found in H. dujardini supports the hypothesis of monochromatic vision in the panarthropod ancestor, whereas two duplications of the ancestral panarthropod c-opsin have led to three c-opsins in tardigrades. Although the early-branching nodes are unstable within the metazoans, our findings suggest that the last common ancestor of Bilateria possessed six opsins: Two r-opsins, one c-opsin, and three Group 4 opsins, one of which (Go opsin) was lost in the ecdysozoan lineage.

Keywords: Panarthropoda; Tardigrada; opsin evolution; transcriptomics; vision.

Fig. 1.—

Visual organs in representatives of Panarthropoda. Although most onychophorans and tardigrades have a pair of simple, ocellus-like eyes (arrows in A and B), arthropods usually show two types of visual organs: The compound eyes (arrowheads in C) and the median ocelli (arrow in C). (A) Scanning electron micrograph of the head of the onychophoran Principapillatus hitoyensis in dorsal view. Scale bar: 1 mm. (B) Light micrograph of the head of the tardigrade Hypsibius dujardini in dorsal view. Scale bar: 10 µm. (C) Stereomicrograph of the head of the hymenopteran Ectemnius cavifrons in dorsal view. Scale bar: 1 mm.

Fig. 2.—

Simplified best obtained ML tree of the full metazoan opsin gene data set and the placement of the five opsin genes from the tardigrade Hypsibius dujardini (highlighted in red). See supplementary figure S1, Supplementary Material online, for the uncondensed tree. (A) Detail view of the bilaterian r-opsin clade, in which Hd-r-opsin of H. dujardini occurs as the sister group to the onychophoran onychopsin clade. (B) Detail view of the neuropsin/opsin-5 subgroup of Group 4 opsins, illustrating the placement of Hd-neuropsin of H. dujardini among the neuropsins from other protostomes. (C) Detail view of the bilaterian c-opsin clade, in which Hd-c-opsin1, Hd-c-opsin2 and Hd-c-opsin3 of H. dujardini are nested as a monophyletic group within the panarthropod c-opsin clade containing the arthropod pteropsins.

Fig. 3.—

Hypotheses on the evolutionary history of opsin genes in Panarthropoda and Bilateria based on our phylogenetic analyses of metazoan opsin sequences. (A) Scenario on opsin evolution in Panarthropoda. The trichotomy is due to the uncertain position of Tardigrada as the sister group of Arthropoda, Onychophora, or Onychophora plus Arthropoda (see Mayer et al. 2013 and references therein). According to this scenario, the last common ancestor of Panarthropoda possessed five opsin genes: One c-opsin, two r-opsins, and two Group 4 opsins. The three c-opsin genes of H. dujardini might have evolved by gene duplications either in the tardigrade lineage, or a tardigrade subgroup. (B) Scenario on opsin evolution in Bilateria, according to which the last common bilaterian ancestor possessed six opsin genes. Although the arthropsin and melanopsin/[visual] r-opsin lineages arose by a duplication of the r-opsin precursor, two additional duplications in the bilaterian Group 4 opsin clade gave rise to the neuropsin/opsin-5, peropsin, and Go-opsin lineages. Note that the Go-opsin gene was subsequently lost in the last common ancestor of Ecdysozoa.