The comb jelly opsins and the origins of animal phototransduction

Abstract

Opsins mediate light detection in most animals, and understanding their evolution is key to clarify the origin of vision. Despite the public availability of a substantial collection of well-characterized opsins, early opsin evolution has yet to be fully understood, in large part because of the high level of divergence observed among opsins belonging to different subfamilies. As a result, different studies have investigated deep opsin evolution using alternative data sets and reached contradictory results. Here, we integrated the data and methods of three, key, recent studies to further clarify opsin evolution. We show that the opsin relationships are sensitive to outgroup choice; we generate new support for the existence of Rhabdomeric opsins in Cnidaria (e.g., corals and jellyfishes) and show that all comb jelly opsins belong to well-recognized opsin groups (the Go-coupled opsins or the Ciliary opsins), which are also known in Bilateria (e.g., humans, fruit flies, snails, and their allies) and Cnidaria. Our results are most parsimoniously interpreted assuming a traditional animal phylogeny where Ctenophora are not the sister group of all the other animals.

Keywords: Ctenophora; Metazoa; comb jelly; evolution; opsin; vision.

Fig. 1.—

Results of the analyses of SEA, SEAm1, and SEAm2 under GTR + G. (a) Results of SEA original data set under GTR + G showing Mnemiopsis3 as the sister of all the other animal opsins. This is the same result that was obtained by Schnitzler et al. (2012) and indicates that model choice, GTR + G here and WAG + G in the study by Schnitzler et al. (2012), is not affecting tree reconstruction. (b) Results of the analysis of the SEA data set but using the MLTs as the only outgroups. In this tree, Mnemiopsis3 is not the sister group of all the other opsins, indicating the importance of outgroup selection in opsin analyses. (c) Results of the analysis of the SEA data set but using the MLTs and placozoans opsin-like sequences (Placopsins) as outgroups. Addition of the Placopsins does not change the relationships of Mnemiopsis3 but allow the recovery of a monophyletic Go-opsin group. Supplementary figure S2, Supplementary Material online, shows that the results of the data sets analyzed in figures 1b and c holds also under WAG + G.

Fig. 2.—

Results of the analyses of FEAm1 under GTR + G. The tree indicates that Mnemiopsis3 is not the sister group of all the other opsins, that Ctenophoran lost their R-opsins and most likely their C-opsins, and that Cnidarians possess R-opsins. Support values are from top to bottom PP (bold values), Sh-like bootstrap, and aBayes bootstrap. Supplementary figures S3, Supplementary Material online, show that the results obtained from the analysis of FEAm1 under GTR + G hold also under WAG + G.