A High Load of Non-neutral Amino-Acid Polymorphisms Explains High Protein Diversity Despite Moderate Effective Population Size in a Marine Bivalve With Sweepstakes Reproduction

Abstract

Marine bivalves show among the greatest allozyme diversity ever reported in Eukaryotes, putting them historically at the heart of the neutralist−selectionist controversy on the maintenance of genetic variation. Although it is now acknowledged that this high diversity is most probably a simple consequence of a large population size, convincing support for this explanation would require a rigorous assessment of the silent nucleotide diversity in natural populations of marine bivalves, which has not yet been done. This study investigated DNA sequence polymorphism in a set of 37 nuclear loci in wild samples of the flat oyster Ostrea edulis. Silent diversity was found to be only moderate (0.7%), and there was no departure from demographic equilibrium under the Wright-Fisher model, suggesting that the effective population size might not be as large as might have been expected. In accordance with allozyme heterozygosity, nonsynonymous diversity was comparatively very high (0.3%), so that the nonsynonymous to silent diversity ratio reached a value rarely observed in any other organism. We estimated that one-quarter of amino acid-changing mutations behave as neutral in O. edulis, and as many as one-third are sufficiently weakly selected to segregate at low frequency in the polymorphism. Finally, we inferred that one oyster is expected to carry more than 4800 non-neutral alleles (or 4.2 cM−1). We conclude that a high load of segregating non-neutral amino-acid polymorphisms contributes to high protein diversity in O. edulis. The high fecundity of marine bivalves together with an unpredictable and highly variable success of reproduction and recruitment (sweepstakes reproduction) might produce a greater decoupling between Ne and N than in other organisms with lower fecundities, and we suggest this could explain why a higher segregating load could be maintained for a given silent mutation effective size.

Genetic inviability is a major driver of type III survivorship in experimental families of a highly fecund marine bivalve

“…A high mutational load in the Pacific oyster is consistent with the very high levels of nucleotide and gap polymorphisms revealed by DNA sequences (Sauvage et al 2007;Harrang et al 2013). SNP frequency across four Pacific oyster genomes is 2.3% , which is >40 times that observed in humans (Sachidanandam et al 2001 but comparable to that in another highly polymorphic marine species, the purple sea urchin (Sodergren et al 2006).…”

“…From vQTL‐mapping data, we estimate per individual wild parent; if we assume that these mutations can occur in n = 5000 genes in Pacific oysters (Harrang et al . ) then the average frequency of these partially dominant lethal mutations is 7.25 × 10 −4 , that is each one is, indeed, expected to be quite rare.…”

“…From classical, mutation-selection, equilibrium theory for partially dominant lethal alleles, assuming selection coefficients, s % 1.0, as previously estimated for recessive viabilityreducing alleles in the oyster (Launey & Hedgecock 2001;Plough & Hedgecock 2011), the number of lethal mutations carried by an individual in a diploid population is n le % 2 qn, where q is the equilibrium frequency of lethal mutations and n is the number of loci at which lethal mutations can arise (Hedrick et al 1999). From vQTL-mapping data, we estimate n le % 7:25 per individual wild parent; if we assume that these mutations can occur in n = 5000 genes in Pacific oysters (Harrang et al 2013) then the average frequency of these partially dominant lethal mutations is 7.25 9 10 À4 , that is each one is, indeed, expected to be quite rare.…”

Swept away: ocean currents and seascape features influence genetic structure across the 18,000 Km Indo-Pacific distribution of a marine invertebrate, the black-lip pearl oyster Pinctada margaritifera

“…Briefly, genome complexity reduction was achieved with a double restriction digest, using a Pst I and Sph I methylation-sensitive restriction enzyme (RE) combination, in a joint digestion-ligation reaction at 37 °C for 2 h with 150–200 ng gDNA. Because P. margaritifera like other bivalve species is highly polymorphic [48, 60], highly repetitive genomic regions were avoided and low copy regions more efficiently targeted for sequence capture with the use of methylation-sensitive REs [61]. …”

Physiological responses of female and male black-lip pearl oysters(Pinctada margaritifera)to different temperatures and concentrations of food

“…It is known that a high level of heterozygosity in marine bivalves is the basis of a wide variability in individual phenotypic responses (Harrang et al 2013). This variability makes it possible to improve growth and stress resistance by genetic selection, which modifies physiological responses such as reproduction (Huvet et al 2010) and immunity (Delaporte et al 2006).…”