Dennis Hedgecock

The sexes of sequentially hermaphroditic cupped oysters are both environmentally and genetically determined. Sex is also associated with growth or body size, females being larger than males of the same age on average. Whether sex determines size or size determines sex has not been resolved. To examine the relationship between growth and sex, 1,360 tagged individuals from six F2 families of Pacific oyster Crassostrea gigas were reared through their second summer in Thorndyke Bay, Washington; individual live weights were recorded for 5 consecutive months, starting in June. At the last weighing, microscopic examination of gonadal tissue revealed four “sexes” in the cohort, females (43% of cohort), males (29%), hermaphrodites (2%), and sex-undetermined individuals with no gametes (26%). Live weights were fit to various sigmoidal growth curves (logistic, Gompertz, and Richards) with fixed and random parameters to account for individual variation. The best fitting curves suggested that growth of the cohort was exponential until late August, when temperatures declined and more than 70% of final weight had been gained. Individual live weights, growth-curve parameters, and growth measures were fit to general linear models with family and sex classification variables. Family-by-sex interaction was significant in many such analyses. Females were larger than males on average and appeared to attain their size advantage from superior growth characteristics rather than from initial size. Males were strikingly either like females or like the smaller sex-undetermined oysters with respect to growth comparisons within family. Sex-undetermined oysters may have been “true” males that were too small to mature as yearlings, though a size-threshold for maturation was not apparent. Genetically determined sex and family genetics appeared to control growth.

Understanding the genetic bases of inbreeding depression, heterosis, and genetic load is integral to understanding how genetic diversity is maintained in natural populations. The Pacific oyster Crassostrea gigas, like many long-lived plants, has high fecundity and high early mortality (type-III survivorship), manifesting a large, overt, genetic load; the oyster harbors an even greater concealed genetic load revealed by inbreeding. Here, we map viability QTL (vQTL) in six interrelated F₂ oyster families, using high-density linkage maps of single nucleotide polymorphisms generated by genotyping-by-sequencing (GBS) methods. Altogether, we detect 70 vQTL and provisionally infer 89 causal mutations, 11 to 20 per family. Genetic mortality caused by independent (unlinked) vQTL ranges from 94.2% to 97.8% across families, consistent with previous reports. High-density maps provide better resolution of genetic mechanisms, however. Models of one causal mutation present in both identical-by-descent (IBD) homozygotes and heterozygotes fit genotype frequencies at 37 vQTL; consistent with the mutation-selection balance theory of genetic load, 20 are highly deleterious, completely recessive mutations and 17 are less deleterious, partially dominant mutations. Another 22 vQTL require pairs of recessive or partially dominant causal mutations, half showing selection against recessive mutations linked in repulsion, producing pseudo-overdominance. Only eight vQTL appear to support the overdominance theory of genetic load, with deficiencies of both IBD homozygotes, but at least four of these are likely caused by pseudo-overdominance. Evidence for epistasis is absent. A high mutation rate, random genetic drift, and pseudo-overdominance may explain both the oyster’s extremely high genetic diversity and a high genetic load maintained primarily by mutation-selection balance.

Studies of linkage and linkage mapping have advanced genetic and biological knowledge for over 100 years. In addition to their growing role, today, in mapping phenotypes to genotypes, dense linkage maps can help to validate genome assemblies. Previously, we showed that 40% of scaffolds in the first genome assembly for the Pacific oyster Crassostrea gigas were chimeric, containing single nucleotide polymorphisms (SNPs) mapping to different linkage groups. Here, we merge 14 linkage maps constructed of SNPs generated from genotyping-by-sequencing (GBS) methods with five, previously constructed linkage maps, to create a compendium of nearly 69 thousand SNPs mapped with high confidence. We use this compendium to assess a recently available, chromosome-level assembly of the C. gigas genome, mapping SNPs in 275 of 301 contigs and comparing the ordering of these contigs, by linkage, to their assembly by Hi-C sequencing methods. We find that, while 26% of contigs contain chimeric blocks of SNPs, i.e. adjacent SNPs mapping to different linkage groups than the majority of SNPs in their contig, these apparent misassemblies amount to only 0.08% of the genome sequence. Furthermore, nearly 90% of 275 contigs mapped by linkage and sequencing are assembled identically; inconsistencies between the two assemblies for the remaining 10% of contigs appear to result from insufficient linkage information. Thus, our compilation of linkage maps strongly supports this chromosome-level assembly of the oyster genome. Finally, we use this assembly to estimate, for the first time in a Lophotrochozoan, genome-wide recombination rates and causes of variation in this fundamental process.

Although aquaculture has grown nearly exponentially over the last six decades, providing 31.6 million metric tons of animal seafood in 2015, its rate of growth has slowed over the last 15 years. Here, we use case studies, drawn mostly from Asian shellfish culture, to suggest that ‘boom‐and‐bust’ production cycles – periods of rapid growth followed by collapse – cause significant losses of seafood production and to illustrate the duration and repetition of boom‐and‐bust cycles. Next, using the global FAO database for aquaculture production from 1950 to 2015, we investigate whether boom‐and‐bust cycles occur more broadly and whether they are playing a role in the declining rate of global aquaculture production. Focusing on FAO production records with maxima before 2011, allowing time for collapse, we categorize production in each record, relative to its maximum value, as sustained, depleted, collapsed or lost. We find 278 of 453 records (61.4%) show collapsed or lost production, although production in most of these records comprises only a tiny fraction of global output. The top 30 records in the collapsed or lost categories do account for 2.4% of cumulative production over the 66‐year record of animal seafood aquaculture. We identify a strong association between short boom phases (5 years or less) and the probability that production will be lost and use this, as well as maximum annual production and year of maximum production, to model the probability of loss. Ecological limits and market problems are the most often discussed causes of boom‐and‐bust production cycles, but we focus, here, on disease as a major proximal cause of collapse and raise the hypothesis that inbreeding depression may often be an ultimate cause by exacerbating disease susceptibility.

The offspring of most highly fecund marine fish and shellfish suffer substantial mortality early in the life cycle, complicating prediction of recruitment and fisheries management. Early mortality has long been attributed to environmental factors and almost never to genetic sources. Previous work on a variety of marine bivalve species uncovered substantial genetic inviability among the offspring of inbred crosses, suggesting a large load of early‐acting deleterious recessive mutations. However, genetic inviability of randomly bred offspring has not been addressed. Here, genome‐wide surveys reveal widespread, genotype‐dependent mortality in randomly bred, full‐sib progenies of wild‐caught Pacific oysters (Crassostrea gigas). Using gene‐mapping methods, we infer that 11–19 detrimental alleles per family render 97.9–99.8% of progeny inviable. The variable genomic positions of viability loci among families imply a surprisingly large load of partially dominant or additive detrimental mutations in wild adult oysters. Although caution is required in interpreting the relevance of experimental results for natural field environments, we argue that the observed genetic inviability corresponds with type III survivorship, which is characteristic of both hatchery and field environments and that our results, therefore, suggest the need for additional experiments under the near‐natural conditions of mesocosms. We explore the population genetic implications of our results, calculating a detrimental mutation rate that is comparable to that estimated for conifers and other highly fecund perennial plants. Genetic inviability ought to be considered as a potential major source of low and variable recruitment in highly fecund marine animals.

The Pacific oyster Crassostrea gigas, a widely cultivated marine bivalve mollusc, is becoming a genetically and genomically enabled model for highly fecund marine metazoans with complex life-histories. A genome sequence is available for the Pacific oyster, as are first-generation, low density, linkage and gene-centromere maps mostly constructed from microsatellite DNA makers. Here, higher density, second-generation, linkage maps are constructed from more than 1100 coding (exonic) single-nucleotide polymorphisms (SNPs), as well as 66 previously mapped microsatellite DNA markers, all typed in five families of Pacific oysters (nearly 172,000 genotypes). The map comprises 10 linkage groups, as expected, has an average total length of 588 centiMorgans (cM), an average marker-spacing of 1.0 cM, and covers 86% of a genome estimated to be 616 cM. All but seven of the mapped SNPs map to 618 genome scaffolds; 260 scaffolds contain two or more mapped SNPs, but for 100 of these scaffolds (38.5%), the contained SNPs map to different linkage groups, suggesting widespread errors in scaffold assemblies. The 100 misassembled scaffolds are significantly longer than those that map to a single linkage group. On the genetic maps, marker orders and inter-marker distances vary across families and mapping methods, owing to an abundance of markers segregating from only one parent, to widespread distortions of segregation ratios caused by early mortality, as previously observed for oysters, and to genotyping errors. Maps made from framework markers provide stronger support for marker orders and reasonable map lengths and are used to produce a consensus high-density linkage map containing 656 markers.