Introduction to the Symposium “Molluscan Models: Advancing Our Understanding of the Eye”

Since the time of Darwin, the eye has been a subject of evolutionary and comparative biologists alike who were intrigued by the structural complexity and morphological diversity of eyes in nature. Much of what we know about the eye—development, structure, physiology, and function—has been determined from only a handful of model organisms, specifically the mouse and the fly. One major phylum in particular, the Mollusca, has been underutilized in investigating the evolution and development of the eye. This is surprising as molluscs display a myriad of eye types, such as simple pit eyes without any apparatus to focus images, compound eyes that superficially resemble the eyes of flies, camera-type eyes that are similar to vertebrate eyes, and eyes with mirrors, just to name a few. As a result, molluscan eyes comprise more morphological diversity than seen even in the largest animal phylum, the Arthropoda

Toward Developing Models to Study the Disease, Ecology, and Evolution of the Eye in Mollusca

Several invertebrate systems have been developed to study various aspects of the eye and eye disease including Drosophila, Planaria, Platynereis, and most recently, the cubozoan jellyfish Tripedalia; however, molluscs, the second largest metazoan phylum, so far have been underrepresented in eye research. This is surprising as mollusc systems offer opportunities to study visual processes that may be altered by disease, vision physiology, development of the visual system, behavior, and evolution. Malacologists have labored for over a century as morphologists, systematists, physiologists, and ecologists in order to understand the structural and functional diversity in molluscs at all levels of biological organization. Yet, malacologists have had little opportunity to interact with researchers whose interests are restricted to the biology and development of eyes as model systems as they tend not to publish in the same journals or attend the same meetings. In an effort to highlight the advantages of molluscan eyes as a model system and encourage greater collaboration among researchers, I provide an overview of molluscan eye research from these two perspectives: eye researchers whose interests involve the development, physiology, and disease of the eye and malacologists who study the complete organism in its natural environment. I discuss the developmental and genetic information available for molluscan eyes and the need to place this work in an evolutionary perspective. Finally, I discuss how synergy between these two groups will advance eye research, broaden research in both fields, and aid in developing new molluscan models for eye research

Congruence and Conflict Between Molecular and Reproductive Characters When Assessing Biological Diversity in the Western Fanshell Cyprogenia aberti (Bivalvia, Unionidae)

Organisms with complex life histories and unusual modes of genome inheritance can present challenges for phylogenetic reconstruction and accurate assessment of biological diversity. This is particularly true for freshwater bivalves in the family Unionidae because: (1) they have complex life cycles that include a parasitic larva and obligate fish host; (2) they possess both a male and female mitochondrial genome that is transmitted through doubly uniparental inheritance (DUI); and (3) they are found in riverine habitats with complex hydrogeological histories. Examination of mitochondrial DNA (mtDNA) sequences, conglutinate morphology, and host fish compatibility of the western fanshell Cyprogenia aberti (Conrad, 1850) revealed significant character variation across its range. Although variation was correlated among the different data sets and supports discrete groups, these groups did not always correspond to geographically isolated populations. Two discrete mtDNA clades exist sympatrically within most C. aberti populations, and these same clades are also diagnosed by at least one morphological character, egg color. The surprisingly high genetic distance (14.61%–20.19%) between the members of these sympatric clades suggests heritance infidelity of the two different mitochondrial genomes. This hypothesis was tested and falsified. More general patterns in geography were observed in host fish compatibility. Populations of C. aberti from the major river systems differed in their ability to utilize fish species as hosts. These differences in reproductive traits, which are presumably genetically based, suggest that these populations are not ecologically exchangeable with one another and represent biological diversity not previously recognized within Cyprogenia Agassiz, 1852

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

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

Convergent and parallel evolution in life habit of the scallops (Bivalvia: Pectinidae)

We employed a phylogenetic framework to identify patterns of life habit evolution in the marine bivalve family Pectinidae. Specifically, we examined the number of independent origins of each life habit and distinguished between convergent and parallel trajectories of life habit evolution using ancestral state estimation. We also investigated whether ancestral character states influence the frequency or type of evolutionary trajectories

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

<p>Abstract</p> <p>Background</p> <p>Duplication 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 <it>Daphnia pulex </it>- 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.</p> <p>Results</p> <p>Using 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.</p> <p>Conclusions</p> <p>Overall, 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.</p

Shell shape convergence masks biological diversity in gliding scallops: description of Ylistrum n. gen. (Pectinidae) from the Indo-Pacific Ocean

The scallop genus Amusium Röding, 1798 is one of few genera of Pectinidae that includes taxa capable of long-distance swimming or gliding. Membership of the genus has been defined primarily by shell shape, and it currently includes only three species: the type species A. pleuronectes (Linnaeus, 1758), A. balloti (Bernardi, 1861) and A. japonicum (Gmelin, 1791). In this study, we use molecular data and aspects of shell morphology to resolve the systematics of the genus. Phylogenetic reconstruction of Pectinidae using nuclear and mitochondrial DNA sequence from four genes supports a polyphyletic Amusium. Differences in internal ribbing pattern provide morphological evidence for the recognition of the two clades identified in our phylogenetic analyses. In contrast, quantification of shell shape through geometric morphometric methods indicates that shape is a convergent phenotype and is not informative in terms of distinguishing between the two gliding lineages. Based on these results, we describe Ylistrum, n. gen, which includes two species previously assigned to Amusium. We provide characters that separate the now monotypic Amusium from the two species, Ylistrum balloti, n. comb. and Y. japonicum, n. comb