Gene duplication and the origins of morphological complexity in pancrustacean eyes, a genomic approach

Abstract

BackgroundDuplication and divergence of genes and genetic networks is hypothesized to be a major driver of the evolution of complexity and novel features. Here, we examine the history of genes and genetic networks in the context of eye evolution by using new approaches to understand patterns of gene duplication during the evolution of metazoan genomes. We hypothesize that 1) genes involved in eye development and phototransduction have duplicated and are retained at higher rates in animal clades that possess more distinct types of optical design; and 2) genes with functional relationships were duplicated and lost together, thereby preserving genetic networks. To test these hypotheses, we examine the rates and patterns of gene duplication and loss evident in 19 metazoan genomes, including that of Daphnia pulex - the first completely sequenced crustacean genome. This is of particular interest because the pancrustaceans (hexapods+crustaceans) have more optical designs than any other major clade of animals, allowing us to test specifically whether the high amount of disparity in pancrustacean eyes is correlated with a higher rate of duplication and retention of vision genes.ResultsUsing protein predictions from 19 metazoan whole-genome projects, we found all members of 23 gene families known to be involved in eye development or phototransduction and deduced their phylogenetic relationships. This allowed us to estimate the number and timing of gene duplication and loss events in these gene families during animal evolution. When comparing duplication/retention rates of these genes, we found that the rate was significantly higher in pancrustaceans than in either vertebrates or non-pancrustacean protostomes. Comparing patterns of co-duplication across Metazoa showed that while these eye-genes co-duplicate at a significantly higher rate than those within a randomly shuffled matrix, many genes with known functional relationships in model organisms did not co-duplicate more often than expected by chance.ConclusionsOverall, and when accounting for factors such as differential rates of whole-genome duplication in different groups, our results are broadly consistent with the hypothesis that genes involved in eye development and phototransduction duplicate at a higher rate in Pancrustacea, the group with the greatest variety of optical designs. The result that these genes have a significantly high number of co-duplications and co-losses could be influenced by shared functions or other unstudied factors such as synteny. Since we did not observe co-duplication/co-loss of genes for all known functional modules (e.g. specific regulatory networks), the interactions among suites of known co-functioning genes (modules) may be plastic at the temporal scale of analysis performed here. Other factors in addition to gene duplication - such as cis-regulation, heterotopy, and co-option - are also likely to be strong factors in the diversification of eye types.

Two temporal functions of Glass: Ommatidium patterning and photoreceptor differentiation

“…Our studies in Drosophila have now described a key regulatory link between rhabdomeric cell type patterning and differentiation mediated by Glass and Pph13. Both of these molecules are conserved in Pancrustaceans (Liu and Friedrich, 2004; Rivera et al, 2010) and homologs can be found in other protostomes including Apylsia californica ((Mahato et al, 2014) and NCBI Ref. Seq.…”

“…Moreover, our studies can serve as the entry point to answer a further question: does this pathway have broader conservation for rhabdomeric differentiation? It is indeed the case that the presence of homologs of Glass and Pph13 were discovered not only in Pancrustaceans, but also in other protostomes such as Aplysia californica , which have a different structural organization of eye in contrast to the compound eye but contain rhabdomeric photoreceptors (Jacklet, 1969; Jacklet et al, 1972; Liu and Friedrich, 2004; Mahato et al, 2014; Rivera et al, 2010). Thus further research on these protostomes will reveal whether Glass-Pph13 interplay acts as an evolutionary ancient transcriptional motif between the morphogenesis of various eye structures and the ensuing differentiation of rhabdomeric photoreceptor neurons.…”

A second visual rhodopsin gene,rh1-2, is expressed in zebrafish photoreceptors and found in other ray-finned fishes

“…While gene duplications have occurred multiple times in invertebrate opsins (Rivera et al, 2010;Serb et al, 2013) and vertebrate cone opsins (Hunt et al, 1998;Matsumoto et al, 2006), visual rhodopsin is generally considered to be a single copy gene, with only a few exceptions. Several eel species have two rhodopsins, one freshwater (rh1fwo) and one marine (rh1dso), and expression shifts from the former to the latter following migration during maturation (Beatty, 1975;Hope et al, 1998;Zhang et al, 2000;Zhang et al, 2002).…”

Blue-light-receptive cryptochrome is expressed in a sponge eye lacking neurons and opsin

“…Using each of the proteins listed above (excluding poriferan and cnidarian sequences) as 'bait' for database searches, we expanded the representation of genes in the phylogenetic analysis employing a pipeline of shell and perl scripts (Rivera et al, 2010;Tong et al, 2009). Each bait sequence from a major photolyase/cryptochrome clade was used to perform similarity searches using BLASTP (Altschul et al, 1997) of two non-redundant protein databases, UniRef50 and UniRef90, curated by UniProt (http://www.uniprot.org/).…”