The Pacific oyster Crassostrea gigas belongs to one of the most species-rich but genomically poorly explored phyla, the Mollusca. Here we report the sequencing and assembly of the oyster genome using short reads and a fosmid-pooling strategy, along with transcriptomes of development and stress response and the proteome of the shell. The oyster genome is highly polymorphic and rich in repetitive sequences, with some transposable elements still actively shaping variation. Transcriptome studies reveal an extensive set of genes responding to environmental stress. The expansion of genes coding for heat shock protein 70 and inhibitors of apoptosis is probably central to the oyster's adaptation to sessile life in the highly stressful intertidal zone. Our analyses also show that shell formation in molluscs is more complex than currently understood and involves extensive participation of cells and their exosomes. The oyster genome sequence fills a void in our understanding of the Lophotrochozoa.Oceans cover approximately 71% of the Earth's surface and harbour most of the phylum diversity of the animal kingdom. Understanding marine biodiversity and its evolution remains a major challenge. The Pacific oyster C. gigas (Thunberg, 1793) is a marine bivalve belonging to the phylum Mollusca, which contains the largest number of described marine animal species 1 . Molluscs have vital roles in the functioning of marine, freshwater and terrestrial ecosystems, and have had major effects on humans, primarily as food sources but also as sources of dyes, decorative pearls and shells, vectors of parasites, and biofouling or destructive agents. Many molluscs are important fishery and aquaculture species, as well as models for studying neurobiology, biomineralization, ocean acidification and adaptation to coastal environments under climate change 2,3 . As the most speciose member of the Lophotrochozoa, phylum Mollusca is central to our understanding of the biology and evolution of this superphylum of protostomes.As sessile marine animals living in estuarine and intertidal regions, oysters must cope with harsh and dynamically changing environments. Abiotic factors such as temperature and salinity fluctuate wildly, and toxic metals and desiccation also pose serious challenges. Filter-feeding oysters face tremendous exposure to microbial pathogens. Oysters do have a notable physical line of defence against predation and desiccation in the formation of thick calcified shells, a key evolutionary innovation making molluscs a successful group. However, acidification of the world's oceans by uptake of anthropogenic carbon dioxide poses a potentially serious threat to this ancient adaptation 4 . Understanding biomineralization and molluscan shell formation is, thus, a major area of interest 5 . Crassostrea gigas is also an interesting model for developmental biology owing to its mosaic development with typical molluscan stages, including trochophore and veliger larvae and metamorphosis.A complete genome sequence of C. gigas would enable a more th...
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We constructed male and female consensus linkage maps for the Pacific oyster Crassostrea gigas, using a total of 102 microsatellite DNA markers typed in 11-day-old larvae from three families. We identified 11 and 12 linkage groups in the male and female consensus maps, respectively. Alignment of these separate maps, however, suggests 10 linkage groups, which agrees with the haploid chromosome number. The male linkage map comprises 88 loci and spans 616.1 cM, while the female map comprises 86 loci and spans 770.5 cM. The male and the female maps share 74 loci; 2 markers remain unlinked. The estimated coverages for the consensus linkage maps are 79% for the male and 70-75% for the female, on the basis of two estimates of genome length. Ninety-five percent of the genome is expected to lie within 16 and 21 cM of markers on the male and female maps, respectively, while 95% of simulated minimum distances to the male and female maps are within 10.1 and 13.6 cM, respectively. Females have significantly more recombination than males, across 118 pairs of linked markers in common to the parents of the three families. Significant differences in recombination and orders of markers are also evident among samesex parents of different families as well as sibling parents of opposite sex. These observations suggest that polymorphism for chromosomal rearrangements may exist in natural populations, which could have profound implications for interpreting the evolutionary genetics of the oyster. These are the first linkage maps for a bivalve mollusc that use microsatellite DNA markers, which should enable them to be transferred to other families and to be useful for further genetic analyses such as QTL mapping.
Inbreeding depression and genetic load have been widely observed, but their genetic basis and effects on fitness during the life cycle remain poorly understood, especially for marine animals with high fecundity and high, early mortality (type-III survivorship). A high load of recessive mutations was previously inferred for the Pacific oyster Crassostrea gigas, from massive distortions of zygotic, marker segregation ratios in F 2 families. However, the number, genomic location, and stage-specific onset of mutations affecting viability have not been thoroughly investigated. Here, we again report massive distortions of microsatellite-marker segregation ratios in two F 2 hybrid families, but we now locate the causative deleterious mutations, using a quantitative trait locus (QTL) interval-mapping model, and we characterize their mode of gene action. We find 14-15 viability QTL (vQTL) in the two families. Genotypic frequencies at vQTL generally suggest selection against recessive or partially recessive alleles, supporting the dominance theory of inbreeding depression. No epistasis was detected among vQTL, so unlinked vQTL presumably have independent effects on survival. For the first time, we track segregation ratios of vQTL-linked markers through the life cycle, to determine their stage-specific expression. Almost all vQTL are absent in the earliest life stages examined, confirming zygotic viability selection; vQTL are predominantly expressed before the juvenile stage (90%), mostly at metamorphosis (50%). We estimate that, altogether, selection on vQTL caused 96% mortality in these families, accounting for nearly all of the actual mortality. Thus, genetic load causes substantial mortality in inbred Pacific oysters, particularly during metamorphosis, a critical developmental transition warranting further investigation.
The great fecundity and very high larval mortality of most marine invertebrates and fish make possible substantial variance in the number of offspring contributed by adults to subsequent generations. The reproductive success of such organisms may thus resemble a sweepstakes lottery, in which a minority of progenitors succeeds in replacing an entire population, while the majority fails to procreate. One specific prediction of this hypothesis, that genetic diversity of newly settled cohorts should be less than that of the adult population, is tested in the present study. Microsatellite DNA markers were examined in naturally spawned juvenile European flat oysters Ostrea edulis (L.), collected over a 12-day period in 1993 from the western Mediterranean Sea, near Sète, France (43°32′N, 3°56′E) and grown out for a period of up to 10 months. Variation in these juveniles was compared to that in a pooled sample of adults collected in 1994 from two locations (Thau Lagoon and Port St. Louis) that had statistically homogeneous allelic frequencies. Though nearly twice as large as the pooled adult sample, the juvenile sample had only 60% of the adult allelic diversity. Analyses of linkage disequilibrium and kinship, as well as estimation of the effective number of parents, suggested that 10-20 adults produced this juvenile cohort. This observation supports the hypothesis of sweepstakes reproductive success and suggests that partial inbreeding may occur even in species with large populations and dispersing planktonic larvae.
Males and females share the same genome, thus, phenotypic divergence requires differential gene expression and sex-specific regulation. Accordingly, the analysis of expression patterns is pivotal to the understanding of sex determination mechanisms. Many bivalves are stable gonochoric species, but the mechanism of gonad sexualization and the genes involved are still unknown. Moreover, during the period of sexual rest, a gonad is not present and sex cannot be determined. A mechanism associated with germ line differentiation in some bivalves, including the Manila clam Ruditapes philippinarum, is the doubly uniparental inheritance (DUI) of mitochondria, a variation of strict maternal inheritance. Two mitochondrial lineages are present, one transmitted through eggs and the other through sperm, as well as a mother-dependent sex bias of the progeny. We produced a de novo annotation of 17,186 transcripts from R. philippinarum and compared the transcriptomes of males and females and identified 1,575 genes with strong sex-specific expression and 166 sex-specific single nucleotide polymorphisms, obtaining preliminary information about genes that could be involved in sex determination. Then we compared the transcriptomes between a family producing predominantly females and a family producing predominantly males to identify candidate genes involved in regulation of sex-specific aspects of DUI system, finding a relationship between sex bias and differential expression of several ubiquitination genes. In mammalian embryos, sperm mitochondria are degraded by ubiquitination. A modification of this mechanism is hypothesized to be responsible for the retention of sperm mitochondria in male embryos of DUI species. Ubiquitination can additionally regulate gene expression, playing a role in sex determination of several animals. These data enable us to develop a model that incorporates both the DUI literature and our new findings.
We characterized 79 microsatellite DNA markers, which were obtained from genomic libraries enriched for CA, GA, ATG and TAGA motif repeats, in the Pacific oyster Crassostrea gigas. For eight F1 grandparents or great‐grandparents of mapping families, the average heterozygosity, 0.705, and average number of alleles per locus, 5.7, did not vary among motif‐repeat or motif‐complexity categories. Non‐amplifying polymerase chain reaction null alleles, which were confirmed by segregation in the mapping families, were detected at 41 (51.9%) of the 79 loci. Cross‐species amplifications from C. angulata, C. sikamea, C. ariakensis and C. virginica showed a precipitous decline with distance from the focal species C. gigas.
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