Nucleotide variation and balancing selection at the Ckma gene in Atlantic cod: analysis with multiple merger coalescent models.

Einar Árnason,Katrín Halldórsdóttir

doi:10.7717/peerj.786

Abstract

High-fecundity organisms, such as Atlantic cod, can withstand substantial natural selection and the entailing genetic load of replacing alleles at a number of loci due to their excess reproductive capacity. High-fecundity organisms may reproduce by sweepstakes leading to highly skewed heavy-tailed offspring distribution. Under such reproduction the Kingman coalescent of binary mergers breaks down and models of multiple merger coalescent are more appropriate. Here we study nucleotide variation at the Ckma (Creatine Kinase Muscle type A) gene in Atlantic cod. The gene shows extreme differentiation between the North (Canada, Greenland, Iceland, Norway, Barents Sea) and the South (Faroe Islands, North-, Baltic-, Celtic-, and Irish Seas) with FST > 0.8 between regions whereas neutral loci show no differentiation. This is evidence of natural selection. The protein sequence is conserved by purifying selection whereas silent and non-coding sites show extreme differentiation. The unfolded site-frequency spectrum has three modes, a mode at singleton sites and two high frequency modes at opposite frequencies representing divergent branches of the gene genealogy that is evidence for balancing selection. Analysis with multiple-merger coalescent models can account for the high frequency of singleton sites and indicate reproductive sweepstakes. Coalescent time scales vary with population size and with the inverse of variance in offspring number. Parameter estimates using multiple-merger coalescent models show that times scales are faster than under the Kingman coalescent.

Highlights

High fecundity translates into large excess reproductive capacity that would allow organisms to withstand substantial natural selection enabling them to bear the entailing high genetic load
The localities are the waters around Newfoundland (New), Greenland (Gre), Iceland (Ice), Faroe Islands (Far), Norway (Nor), and the Barents Sea (Bar), North Sea (Nse), Celtic Sea (Cel), Irish Sea (Iri), Baltic Sea (Bal), and the White Sea (Whi)
If the time of separation of G. morhua and G. macrocephalus and G. chalcogrammus is taken at 3.8–4.0 Mya (Coulson et al, 2006) the time of separation of the A and B clades would be 2 Mya based on the nucleotide divergence of the A and B clades which we show is one half that of the closely related taxa

Summary

Introduction

High fecundity translates into large excess reproductive capacity that would allow organisms to withstand substantial natural selection enabling them to bear the entailing high genetic load. Trying to explain the paradox of sexual reproduction Williams (1975) in his Sex and Evolution book argues that high-fecundity coupled with heavy mortality of young. (type III survivorship) may be able to pay the 50% fitness cost of meiosis. He developed several models, such as the Elm/Oyster and the Cod/Starfish models, which emphasize the importance of high-fecundity for selection. There is no heritability of fitness and sexual reproduction continuously assembles Sisyphean genotypes (from Sisyphus who was punished to roll a boulder up a hill only to see it roll back down, and having to repeat his actions forever). The distribution of offspring numbers is highly skewed, heavy-tailed and with high variance (lognormal). Neutral variation will drift faster under pervasive natural selection

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Conclusion