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Many marine organisms have a biphasic life cycle that transitions between a swimming larva with a more sedentary adult form. At the end of the first phase, larvae must identify suitable sites to settle and undergo a dramatic morphological change. Environmental factors, including photic and chemical cues, appear to influence settlement, but the sensory receptors involved are largely unknown. We targeted the protein receptor, opsin, which belongs to large superfamily of transmembrane receptors that detects environmental stimuli, hormones, and neurotransmitters. While opsins are well-known for light-sensing, including vision, a growing number of studies have demonstrated light-independent functions. We therefore examined opsin expression in the Pteriomorphia, a large, diverse clade of marine bivalves, that includes commercially important species, such as oysters, mussels, and scallops. Methods Genomic annotations combined with phylogenetic analysis show great variation of opsin abundance among pteriomorphian bivalves, including surprisingly high genomic abundance in many species that are eyeless as adults, such as mussels. Therefore, we investigated the diversity of opsin expression from the perspective of larval development. We collected opsin gene expression in four families of Pteriomorphia, across three distinct larval stages, i.e., trochophore, veliger, and pediveliger, and compared those to adult tissues.Results We found larvae express all opsin types in these bivalves, but opsin expression patterns are largely species-specific across development. Few opsins are expressed in the adult mantle, but many are highly expressed in adult eyes. Intriguingly, opsin genes such as retinochrome, xenopsins, and Go-opsins have higher levels of expression in the later larval stages when substrates for settlement are being tested, such as the pediveliger. Conclusion Investigating opsin gene expression during larval development provides crucial insights into their intricate interactions with the surroundings, which may shed light on how opsin receptors of these organisms respond to various environmental cues that play a pivotal role in their settlement process. 

Abstract In animals, opsins and cryptochromes are major protein families that transduce light signals when bound to light-absorbing chromophores. Opsins are involved in various light-dependent processes, like vision, and have been co-opted for light-independent sensory modalities. Cryptochromes are important photoreceptors in animals, generally regulating circadian rhythm, they belong to a larger protein family with photolyases, which repair UV-induced DNA damage. Mollusks are great animals to explore questions about light sensing as eyes have evolved multiple times across, and within, taxonomic classes. We used molluscan genome assemblies from 80 species to predict protein sequences and examine gene family evolution using phylogenetic approaches. We found extensive opsin family expansion and contraction, particularly in bivalve xenopsins and gastropod Go-opsins, while other opsins, like retinochrome, rarely duplicate. Bivalve and gastropod lineages exhibit fluctuations in opsin repertoire, with cephalopods having the fewest number of opsins and loss of at least 2 major opsin types. Interestingly, opsin expansions are not limited to eyed species, and the highest opsin content was seen in eyeless bivalves. The dynamic nature of opsin evolution is quite contrary to the general lack of diversification in mollusk cryptochromes, though some taxa, including cephalopods and terrestrial gastropods, have reduced repertoires of both protein families. We also found complete loss of opsins and cryptochromes in multiple, but not all, deep-sea species. These results help set the stage for connecting genomic changes, including opsin family expansion and contraction, with differences in environmental, and biological features across Mollusca. 

ABSTRACT The relationship between genotype and phenotype is non-trivial because of the often complex molecular pathways that make it difficult to unambiguously relate phenotypes to specific genotypes. Photopigments, comprising an opsin apoprotein bound to a light-absorbing chromophore, present an opportunity to directly relate the amino acid sequence to an absorbance peak phenotype (λmax). We examined this relationship by conducting a series of site-directed mutagenesis experiments of retinochrome, a non-visual opsin, from two closely related species: the common bay scallop, Argopecten irradians, and the king scallop, Pecten maximus. Using protein folding models, we identified three amino acid sites of likely functional importance and expressed mutated retinochrome proteins in vitro. Our results show that the mutation of amino acids lining the opsin binding pocket is responsible for fine spectral tuning, or small changes in the λmax of these light-sensitive proteins. Mutations resulted in a blue or red shift as predicted, but with dissimilar magnitudes. Shifts ranged from a 16 nm blue shift to a 12 nm red shift from the wild-type λmax. These mutations do not show an additive effect, but rather suggest the presence of epistatic interactions. This work highlights the importance of binding pocket shape in the evolution of spectral tuning and builds on our ability to relate genotypic changes to phenotypes in an emerging model for opsin functional analysis. 

Tentacles are fascinating, multifunctional organs found in many aquatic invertebrate groups. In bivalves, tentacles are morphologically diverse, performing protective and sensory roles in taxa from different ecological niches. Such diversity is particularly accentuated in Pteriomorphia, a clade comprising scallops, oysters, file clams, and relatives. However, little is known about the evolution of these organs and their role in bivalve radiation. To test hypotheses of convergent tentacular evolution and a possible association between tentacles and body orientation on the substrate, we first examined tentacle morphology in 108 preserved species representing 15 families across Pteriomorphia. Morphological descriptions of tentacle type (inner mantle fold tentacles, IFT; middle mantle fold tentacles, MFT) and position (marginal and submarginal) are provided, expanding the knowledge of less studied bivalve taxa. Then, we placed the morphological dataset under a molecular phylogenetic framework to estimate ancestral states. IFT had likely four independent origins, while MFT emerged twice independently. After being gained, tentacles have not been lost. In addition, evolution of MFT coincides with transitions in body position with the midsagittal plane parallel to the substrate in the clades of scallops (Pectinida) and oysters (Ostreida). Such a shift could be related to the increase of mantle exposure, favoring the emergence of serially repeated organs, such as tentacles. Altogether, our results support the convergent evolution of tentacles across different taxonomic levels, corroborating the plasticity of the molluscan body and the relevance of evolutionary convergences in the radiation of bivalves. 

Abstract Convergent morphology is a strong indication of an adaptive trait. Marine mussels (Mytilidae) have long been studied for their ecology and economic importance. However, variation in lifestyle and phenotype also make them suitable models for studies focused on ecomorphological correlation and adaptation. The present study investigates mantle margin diversity and ecological transitions in the Mytilidae to identify macroevolutionary patterns and test for convergent evolution. A fossil-calibrated phylogenetic hypothesis of Mytilidae is inferred based on five genes for 33 species (19 genera). Morphological variation in the mantle margin is examined in 43 preserved species (25 genera) and four focal species are examined for detailed anatomy. Trait evolution is investigated by ancestral state estimation and correlation tests. Our phylogeny recovers two main clades derived from an epifaunal ancestor. Subsequently, different lineages convergently shifted to other lifestyles: semi-infaunal or boring into hard substrate. Such transitions are correlated with the development of long siphons in the posterior mantle region. Two independent origins are reconstructed for the posterior lobules on the inner fold, which are associated with intense mucociliary transport, suggesting an important cleansing role in epifaunal mussels. Our results reveal new examples of convergent morphological evolution associated with lifestyle transitions in marine mussels.