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Mitochondrial DNA hyperdiversity and population genetics in the periwinkle Melarhaphe neritoides (Mollusca: Gastropoda)

par Fourdrilis, Severine
Président du jury Noret, Nausicaa
Promoteur Mardulyn, Patrick ;Backeljau, Thierry
Publication Non publié, 2017-06-28

Thèse de doctorat

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Résumé :

This PhD thesis studies the evolution of the peculiar mitochondrial DNA (mtDNA) in the mollusc Melarhaphe neritoides. We measured mtDNA diversity and elucidated the evolutionary forces that shape the evolution of the organelle.The mtDNA in M. neritoides harbours a remarkable amount of polymorphism at selectively neutral nucleotide sites (π_syn = 6.8 %), called hyperdiversity when above the threshold of 5 %. We revealed that an elevated mutation rate (µ = 5.8 × 10-5 per site per year at the COI locus), which is 1000 fold higher than in other metazoans, is likely the primary force generating mtDNA hyperdiversity. Such mtDNA hyperdiversity may be more common across other phyla and more frequently linked to high µ values, than currently appreciated.Natural selection is a second force, which shapes mtDNA hyperdiversity. Positive selection influences the overall mtDNA polymorphism in the 16S, COI and Cytb genes, including synonymous sites at which mtDNA hyperdiversity is calculated. Therefore, synonymous sites in M. neritoides are not neutral but possibly positively selected. Strong purifying selection maintains a low non-synonymous polymorphism in the 13 protein-coding genes of the mitogenome, so that a very few changes in nucleotide sequence induce changes in amino acid sequence. The effective population size of this planktonic-dispersing species is surprisingly small in the North East Atlantic (Ne = 1303), likely biased by selection, and for this reason, Ne is a poor indicator of mtDNA hyperdiversity.Migration is a third force, which homogenises the gene pool of the species through high rates of gene flow, predominantly eastward, and results in high connectivity and panmixia over the entire North East Atlantic.Genetic drift, the fourth force, is not sufficient in M. neritoides to lower mtDNA diversity, and populations show no differentiation.This thesis also highlights an important pitfall. The use of hyperdiverse markers may easily lead to erroneous interpretations of differentiation statistics and connectivity pattern, due to the lack of shared haplotypes in datasets induced by a high µ. First, D_EST may reach a maximal value of 1 but is not indicative of differentiation in terms of fixation (D_EST = 1 ≠ φ_ST = 1), and only reflects differentiation in terms of lack of shared haplotypes. Second, the signal of gene flow is concealed in haplotype network bush-like pattern.Rapid evolution of mtDNA results in significant selection pressure for co-adaptation of the nuclear genome encoding mitochondrial proteins. The elevated µ underlying mtDNA hyperdiversity provides an interesting framework for better understanding how mutational dynamics and selection that drive mitonuclear coevolution contribute to speciation.