A rapidly evolving secretome builds and patterns a sea shell.
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BACKGROUND: Instructions to fabricate mineralized structures with distinct nanoscale architectures, such as seashells and coral and vertebrate skeletons, are encoded in the genomes of a wide variety of animals. In mollusks, the mantle is responsible for the extracellular production of the shell, directing the ordered biomineralization of CaCO3 and the deposition of architectural and color patterns. The evolutionary origins of the ability to synthesize calcified structures across various metazoan taxa remain obscure, with only a small number of protein families identified from molluskan shells. The recent sequencing of a wide range of metazoan genomes coupled with the analysis of gene expression in non-model animals has allowed us to investigate the evolution and process of biomineralization in gastropod mollusks. RESULTS: Here we show that over 25% of the genes expressed in the mantle of the vetigastropod Haliotis asinina encode secreted proteins, indicating that hundreds of proteins are likely to be contributing to shell fabrication and patterning. Almost 85% of the secretome encodes novel proteins; remarkably, only 19% of these have identifiable homologues in the full genome of the patellogastropod Lottia scutum. The spatial expression profiles of mantle genes that belong to the secretome is restricted to discrete mantle zones, with each zone responsible for the fabrication of one of the structural layers of the shell. Patterned expression of a subset of genes along the length of the mantle is indicative of roles in shell ornamentation. For example, Has-sometsuke maps precisely to pigmentation patterns in the shell, providing the first case of a gene product to be involved in molluskan shell pigmentation. We also describe the expression of two novel genes involved in nacre (mother of pearl) deposition. CONCLUSION: The unexpected complexity and evolvability of this secretome and the modular design of the molluskan mantle enables diversification of shell strength and design, and as such must contribute to the variety of adaptive architectures and colors found in mollusk shells. The composition of this novel mantle-specific secretome suggests that there are significant molecular differences in the ways in which gastropods synthesize their shells. (+info)
Host shift and speciation in a coral-feeding nudibranch.
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While the role of host preference in ecological speciation has been investigated extensively in terrestrial systems, very little is known in marine environments. Host preference combined with mate choice on the preferred host can lead to population subdivision and adaptation leading to host shifts. We use a phylogenetic approach based on two mitochondrial genetic markers to disentangle the taxonomic status and to investigate the role of host specificity in the speciation of the nudibranch genus Phestilla (Gastropoda, Opisthobranchia) from Guam, Palau and Hawaii. Species of the genus Phestilla complete their life cycle almost entirely on their specific host coral (species of Porites, Goniopora and Tubastrea). They reproduce on their host coral and their planktonic larvae require a host-specific chemical cue to metamorphose and settle onto their host. The phylogenetic trees of the combined cytochrome oxidase I and ribosomal 16S gene sequences clarify the relationship among species of Phestilla identifying most of the nominal species as monophyletic clades. We found a possible case of host shift from Porites to Goniopora and Tubastrea in sympatric Phestilla spp. This represents one of the first documented cases of host shift as a mechanism underlying speciation in a marine invertebrate. Furthermore, we found highly divergent clades within Phestilla sp. 1 and Phestilla minor (8.1-11.1%), suggesting cryptic speciation. The presence of a strong phylogenetic signal for the coral host confirms that the tight link between species of Phestilla and their host coral probably played an important role in speciation within this genus. (+info)
Linkage maps for the Pacific abalone (genus Haliotis) based on microsatellite DNA markers.
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This study presents linkage maps for the Pacific abalone (Haliotis discus hannai) based on 180 microsatellite DNA markers. Linkage mapping was performed using three F1 outbred families, and a composite linkage map for each sex was generated by incorporating map information from the multiple families. A total of 160 markers are placed on the consolidated female map and 167 markers on the male map. The numbers of linkage groups in the composite female and male maps are 19 and 18, respectively; however, by aligning the two maps, 18 linkage groups are formed, which are consistent with the haploid chromosome number of H. discus hannai. The female map spans 888.1 cM (Kosambi) with an average spacing of 6.3 cM; the male map spans 702.4 cM with an average spacing of 4.7 cM. However, we encountered several linkage groups that show a high level of heterogeneity in recombination rate between families even within the same sex, which reduces the precision of the consolidated maps. Nevertheless, we suggest that the composite maps are of significant potential use as a scaffold to further extend the coverage of the H. discus hannai genome with additional markers. (+info)
Development of embryonic and larval cells containing serotonin, catecholamines, and FMRFamide-related peptides in the gastropod mollusc Phestilla sibogae.
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The present immunocytochemical study provides one of the first detailed descriptions of the development of cells containing a variety of neurotransmitters during much of the larval life of a nudibranch gastropod. Throughout much of early development, serotonergic cells were located only in the apical organ; as larvae approached metamorphosis, serotonergic cells were also detected in the cerebropleural and pedal ganglia. Cells exhibiting tyrosine hydroxylase immunoreactivity (indicative of catecholamine synthesis) were first located near the mouth but by late embryonic stages were also located in the apical organ and near the velum and eyes. By late larval stages, numerous catecholaminergic cells were found in the foot, with concentrations in the propodium. Finally, the first cells exhibiting FMRFamide immunoreactivity were detected posterior to the neuropil of the cerebropleural ganglia in the early embryo. Fibers that presumably originated from these cells subsequently invaded the cerebral and pedal ganglia and the apical organ. By early larval stages, a second pair of peptidergic neurons was located near the first pair, and additional peptidergic neurons were located in the apical organ and peripheral positions in the foot and medial and dorsal to the eyes. In addition to providing a unique phyletic perspective to our understanding of gastropod neural development, the present study also sets the stage for future studies into changes in the nervous system as this gastropod undergoes metamorphosis. (+info)
PCR-based detection of Angiostrongylus cantonensis in tissue and mucus secretions from molluscan hosts.
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Angiostrongylus cantonensis is a common cause of human eosinophilic meningitis. Recent outbreaks of this infection have shown that there is a need to determine the distribution of this nematode in the environment in order to control transmission. A. cantonensis is generally identified morphologically in the molluscan intermediate host by microscopic examination, which can be labor-intensive. The aim of this study was to develop a PCR-based method to detect A. cantonensis directly from molluscan tissue. A total of 34 Parmarion cf. martensi (Simroth) semislugs, 25 of which were naturally infected with A. cantonensis, were used to develop this assay. Tissue pieces (approximately 25 mg) were digested with pepsin-HCl to recover third-stage larvae for morphological identification or were used for DNA extraction. PCR primers were designed to amplify 1,134 bp from the Angiostrongylus 18S rRNA gene, and the amplicons produced were sequenced for identification at the species level. Both microscopy and the PCR-DNA sequencing analysis indicated that the same 25 semislugs were positive for A. cantonensis, showing that the two methods were equally sensitive and specific for this application. However, morphological detection requires access to living mollusks, whereas molecular analysis can also be performed with frozen tissue. The PCR-DNA sequencing method was further evaluated using tissue from Veronicella cubensis (Pfeiffer) slugs and mucus secretions from infected P. martensi. To our knowledge, this is the first use of a PCR-based method to confirm the presence of A. cantonensis in mollusks collected in the environment. (+info)
Precopulatory stabbing, hypodermic injections and unilateral copulations in a hermaphroditic sea slug.
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Reciprocity constitutes the prevalent mating mechanism among simultaneous hermaphrodites. Yet, when copulations in the female role confer fitness costs through male manipulation, it becomes advantageous sometimes to mate unilaterally in the male role only. In the sea slug Siphopteron quadrispinosum, acting males stab their partner with a bipartite penis, which not only hypodermically injects prostate fluids, but also apparently mechanically enforces unilateral male matings. Despite a pronounced male mating drive in both partners, unilaterality ensued when one slug stabbed more rapidly than its partner. The acting male may thus avoid the costs inflicted by traumatic injections and penial spines. While future studies need to elucidate the net fitness consequences of stabbing, our behavioural evidence is in line with the hypothesis that mating in S. quadrispinosum represents conflicting rather than complementary mating interests between mates. (+info)
The dynamics of nacre self-assembly.
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We show how nacre and pearl construction in bivalve and gastropod molluscs can be understood in terms of successive processes of controlled self-assembly from the molecular- to the macro-scale. This dynamics involves the physics of the formation of both solid and liquid crystals and of membranes and fluids to produce a nanostructured hierarchically constructed biological composite of polysaccharides, proteins and mineral, whose mechanical properties far surpass those of its component parts. (+info)
Reticulate phylogeny of gastropod-shell-breeding cichlids from Lake Tanganyika--the result of repeated introgressive hybridization.
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BACKGROUND: The tribe Lamprologini is the major substrate breeding lineage of Lake Tanganyika's cichlid species flock. Among several different life history strategies found in lamprologines, the adaptation to live and breed in empty gastropod shells is probably the most peculiar. Although shell-breeding arose several times in the evolutionary history of the lamprologines, all obligatory and most facultative shell-breeders belong to the so called "ossified group", a monophyletic lineage within the lamprologine cichlids. Since their distinctive life style enables these species to live and breed in closest vicinity, we hypothesized that these cichlids might be particularly prone to accidental hybridization, and that introgression might have affected the evolutionary history of this cichlid lineage. RESULTS: Our analyses revealed discrepancies between phylogenetic hypotheses based on mitochondrial and nuclear (AFLP) data. While the nuclear phylogeny was congruent with morphological, behavioral and ecological characteristics, several species--usually highly specialized shell-breeders--were placed at contradicting positions in the mitochondrial phylogeny. The discordant phylogenies strongly suggest repeated incidents of introgressive hybridization between several distantly related shell-breeding species, which reticulated the phylogeny of this group of cichlids. Long interior branches and high bootstrap support for many interior nodes in the mitochondrial phylogeny argue against a major effect of ancient incomplete lineage sorting on the phylogenetic reconstruction. Moreover, we provide morphological and genetic (mtDNA and microsatellites) evidence for ongoing hybridization among distantly related shell-breeders. In these cases, the territorial males of the inferred paternal species are too large to enter the shells of their mate, such that they have to release their sperm over the entrance of the shell to fertilize the eggs. With sperm dispersal by water currents and wave action, trans-specific fertilization of clutches in neighboring shells seem inevitable, when post-zygotic isolation is incomplete. CONCLUSION: From the direct observation of hybrids we conclude that hybridization between distantly related gastropod-shell-breeding cichlids of Lake Tanganyika follows inevitably from their ecological specialization. Moreover, the observed incongruence between mtDNA and nuclear multilocus phylogeny suggests that repeated hybridization events among quite distantly related taxa affected the diversification of this group, and introduced reticulation into their phylogeny. (+info)