Deep Diversity: Extensive Variation in the Components of Complex Visual Systems across Animals

Abstract

Understanding the molecular underpinnings of the evolution of complex (multi-part) systems is a fundamental topic in biology. One unanswered question is to what the extent do similar or different genes and regulatory interactions underlie similar complex systems across species? Animal eyes and phototransduction (light detection) are outstanding systems to investigate this question because some of the genetics underlying these traits are well characterized in model organisms. However, comparative studies using non-model organisms are also necessary to understand the diversity and evolution of these traits. Here, we compare the characteristics of photoreceptor cells, opsins, and phototransduction cascades in diverse taxa, with a particular focus on cnidarians. In contrast to the common theme of deep homology, whereby similar traits develop mainly using homologous genes, comparisons of visual systems, especially in non-model organisms, are beginning to highlight a “deep diversity” of underlying components, illustrating how variation can underlie similar complex systems across taxa. Although using candidate genes from model organisms across diversity was a good starting point to understand the evolution of complex systems, unbiased genome-wide comparisons and subsequent functional validation will be necessary to uncover unique genes that comprise the complex systems of non-model groups to better understand biodiversity and its evolution.

Multiple parallel expansions of bilaterian-like phototransduction gene families in the eyeless Anthozoa

“…5A). This confirms previous research indicating cnidarians only have these three AC types (Vöcking et al 2022). AC3 and AC5/6 are likely candidates in the phototransduction cascade in N. vectensis, possibly through cnidopsin signaling.…”

“…7A, Fig. S8) (Peng et al, 2015; Vöcking et al, 2022). We find that previously identified cnidarian TRPCs are split into two groups, one of which is pan-cnidarian, while the other is anthozoan-specific (Fig.…”

“…The N. vectensis candidate protein sequences were also searched in the genome assemblies of Alatina alata (Ohdera et al, 2019) and Aurelia aurita (Gold et al, 2019), and the top query hits were saved. Additional sequences were obtained from alignments from (Krishnan et al, 2015; Lagman et al, 2022; Moroz et al, 2023; Peng et al, 2015; Vöcking et al, 2022) and redundant sequences were not included.…”

“…For the G protein □ genes, N. vectensis sequences were retrieved from Interpro (Paysan-Lafosse et al, 2023) using the domain accession numbers PS50058 and PF00631. Adenylyl cyclase sequences were retrieved from (Vöcking et al, 2022) and used as bait to search on NCBI BLAST in the species listed previously.…”

“…Cnidaria are sister to Bilateria and offer an important phylogenetic comparison to understand the evolution of complexity in animals. The few comparative studies on phototransduction in Cnidaria have almost exclusively focused on jellyfish and Hydra (Medusozoa) (Ekström et al, 2008; Plachetzki et al, 2010; Vöcking et al, 2022) Evidence in box jellies suggests that a Gαs subunit signals via the non-canonical AC enzyme, similar to bilaterian tetraopsin signaling (Koyanagi et al, 2008). In addition, cnidarians with eyes share many of the same molecular components as bilaterian eyes, such as developmental genes, phototransduction cascade members, and opsins (Kozmik et al, 2008).…”