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

Type Article
Date 2013-02
Language English
Author(s) Harrang Estelle1, Lapegue SylvieORCID1, Morga BenjaminORCID1, Bierne Nicolas2, 3
Affiliation(s) 1 : IFREMER, Lab Genet & Pathol, F-17390 La Tremblade, France.
2 : Univ Montpellier 2, F-34095 Montpellier 2, France.
3 : CNRS, Inst Sci Evolut, Stn Mediterraneenne Environm Littoral, UMR5554, F-34200 Sete, France.
Source G3-genes Genomes Genetics (2160-1836) (Genetics Soc Am), 2013-02 , Vol. 3 , N. 2 , P. 333-341
DOI 10.1534/g3.112.005181
WOS© Times Cited 21
Keyword(s) nucleotide polymorphism, marine bivalve, deleterious mutations, genetic load, Ostrea edulis
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.
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Harrang Estelle, Lapegue Sylvie, Morga Benjamin, Bierne Nicolas (2013). 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. G3-genes Genomes Genetics, 3(2), 333-341. Publisher's official version : https://doi.org/10.1534/g3.112.005181 , Open Access version : https://archimer.ifremer.fr/doc/00125/23610/