An unusual case of gender-associated mitochondrial DNA heteroplasmy: the mytilid Musculista senhousia (Mollusca Bivalvia)

Abstract

Background: Doubly Uniparental Inheritance (DUI) represents the most outstanding exception to matrilinear inheritance of mitochondrial DNA (mtDNA), typical of Metazoa. In a few bivalve mollusks, two sex-linked mtDNAs (the so-called M and F) are inherited in a peculiar way: both daughters and sons receive their F from the mother, whereas sons inherit M from the father (males do not transmit F to their progeny). This realizes a double mechanism of transmission, in which M and F mtDNAs are inherited uniparentally. DUI systems represent a unique experimental model for testing the evolutionary mechanisms that apply to mitochondrial genomes and their transmission patterns as well as to mtDNA recombination.

Results: A new case of DUI is described in Musculista senhousia (Mollusca: Bivalvia: Mytilidae). Its heteroplasmy pattern is in line with standard DUI. Sequence variability analysis evidenced two main results: F haplotypes sequence variability is higher than that of M haplotypes, and F mitochondrial haplotypes experience a higher mutation rate in males' somatic tissues than in females' ones. Phylogenetic analysis revealed also that M. senhousia M and F haplotypes cluster separately from that of the other mytilids.

Conclusion: Sequence variability analysis evidenced some unexpected traits. The inverted variability pattern (the F being more variable than M) was new and it challenges most of the rationales proposed to account for sex-linked mtDNA evolution. We tentatively related this to the history of the Northern Adriatic populations analyzed. Moreover, F sequences evidenced a higher mutation level in male's soma, this variability being produced de novo each generation. This suggests that mechanisms evolved to protect mtDNA in females (f.i. antioxidant gene complexes) might be under relaxed selection in males. Phylogenetic analysis of sex-linked haplotypes confirmed that they have switched their roles during the evolutionary history of mytilids, at variance to what has been observed in unionids. Consequently, reciprocal monophyly of M and F lineages got easily lost because of role-reversals and consequent losses of M lineages, as already observed in Mytilus.

Figure 1

Sequence variability from gametes. Mean values and graph of sequence variability (p-distance) of M. senhousia sex-linked haplotypes obtained from gametes. Mean and standard error values of nucleotide p-distances are reported for cob, cox1 and rrnL mitochondrial genes. Levels of significance were obtained by random resampling. F, female haplotypes in eggs; M, male haplotypes in sperm; pD, nucleotide p-distance; SE, standard error; *, significant.

Figure 2

Sequence variability from somatic tissues. Mean values and graph of sequence variability (p-distance) of M. senhousia sex-linked haplotypes obtained from somatic tissues and comparisons with the gonads. Mean and standard error values of nucleotide p-distances are reported for cob mitochondrial gene. Levels of significance were obtained by random resampling. F, female haplotypes in eggs; M, male haplotypes in sperm; pD, nucleotide p-distance; SE, standard error; *, significant.

Figure 3

Phylogenetic inference of DUI-related mitochondrial types. Maximum Likelihood trees based on rrnL (A) and cox1 (B) mitochondrial genes, showing phyletic relationships of Musculista senhousia sex-linked haplotypes to other DUI species (Mytilus spp., Geukensia demissa, – Mytilidae; Fusconaia flava – Unionidae; Tapes philippinarum – Veneridae). Figures above branches indicate bootstrap values (100 replicates). Whenever available, GenBank accession numbers are reported on taxon labels. * Mytilus trossulus M cox1 sequence is not available in GenBank and it has been obtained from [52].